Aneurysms of the Vertebral and Posterior Inferior Cerebellar Arteries

Aneurysms of the vertebral and posterior inferior cerebellar arteries

Hanna Lehto, MD

Department of Neurosurgery Helsinki University Central Hospital Helsinki, Finland

and

Faculty of Medicine University of Helsinki Helsinki, Finland

Academic Dissertation

To be publicly discussed with the permission of the Faculty of Medicine of the University of Helsinki, in Lecture Hall 1 of Töölö Hospital on April 17th 2015, at 12 noon.

Vkirja_viite_255246_LEHTO_.indd 3 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 2 30.3.2015 15.09 Supervisors: Professor Juha Hernesniemi Department of Neurosurgery Helsinki University Central Hospital Helsinki, Finland

Associate Professor Mika Niemelä Department of Neurosurgery Helsinki University Central Hospital Helsinki, Finland

Reviewers: Associate Professor Timo Kumpulainen Department of Neurosurgery Oulu University Hospital Oulu, Finland

Associate Professor Topi Siniluoto Deparment of Radiology Oulu University Hospital Oulu, Finland

Opponent: Professor Andreas Gruber Department of Neurosurgery Medical University of Vienna Vienna, Austria

ISBN 978-951-51-0901-9 (paperback) ISBN 978-951-51-0902-6 (PDF) http://ethesis.helsinki.fi Unigrafia, Helsinki, 2015

Vkirja_viite_255246_LEHTO_.indd 3 30.3.2015 15.09 Table of contents

Original publications...... 9 Abbreviations...... 11 Abstract...... 13

17 Introduction

21 Review of the literature Cerebral artery aneurysms and subarachnoid hemorrhage...... 21 Incidence and prevalence...... 21 Diagnostics...... 21 Risk Factors ...... 21 Morphology and etiology...... 21 Histology...... 22 Genetics...... 22 Treatment...... 22 Outcome...... 23 Preventive treatment...... 23 Posterior circulation aneurysms...... 24 Definition...... 24 Incidence...... 24 Location...... 24 Special features compared to anterior circulation...... 24 History of treatment...... 24 The vertebral artery and the posterior inferior cerebellar artery...... 27 Anatomy...... 27 Controversies in nomenclature...... 31 Aneurysms...... 31 Treatment...... 35 Outcome...... 37

41 Aims of the study

43 Patients and methods Patients...... 43 Data and analysis...... 44 Radiological data...... 44 Follow-up data...... 45 Statistical analysis...... 45

Vkirja_viite_255246_LEHTO_.indd 4 30.3.2015 15.09 47 Results Incidence of vertebral and posterior inferior cerebellar artery aneurysms...... 47 Anatomy of aneurysms at junction of the vertebral artery and the posterior inferior cerebellar artery...... 47 Patients and aneurysms...... 47 PICA aneurysms...... 47 Variations of VA and PICA...... 48 Jugular tubercle...... 48 Overview of patients with vertebral artery or posterior inferior cerebellar artery aneurysms...... 51 Patients and aneurysms...... 51 Treatment...... 52 Outcome...... 56 Patients with ruptured vertebral or posterior inferior cerebellar artery aneurysms...... 60 Patients and aneurysms...... 60 Treatment and angiographic outcome...... 63 Clinical outcome...... 64 Patients with unruptured vertebral artery or posterior inferior cerebellar artery aneurysms...... 72 Overview...... 72 Ruptured aneurysm in another location...... 72 Ruptured arteriovenous malformation...... 76 Mass effect...... 76 Ischemia...... 77 Incidental aneurysms...... 78

81 Discussion Incidence...... 81 Anatomic features...... 81 Location...... 81 Morphology...... 82 Anatomy of VA–PICA aneurysms in CTA...... 82 Treatment...... 82 Surgical treatment and radiological outcome...... 83 endovascular treatment and radiological outcome...... 83 Choosing the treatment modality and techniques ...... 84 Outcome ...... 84 Future perspectives ...... 84 etiology of VA and distal PICA aneurysms...... 84 Future treatment...... 84 Conclusion...... 85

Acknowlwdgement...... 87 Literature...... 91 original publications...... 111

Vkirja_viite_255246_LEHTO_.indd 5 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 6 30.3.2015 15.09 Original publications

I Lehto H, Kivisaari R, Niemelä M, Dashti R, Elsharkawy A, Harati A, Satopää J, Koroknay-Pál P, Laakso A, Hernesniemi J.: Seventy Aneurysms of the Posterior Inferior Cerebellar Artery: Anatomical Features and Value of Computed Tomography Angiography in Microneuro-surgery. World Neurosurgery, 2014 82(6):1106 – 1112

II Lehto H, Harati A, Niemelä M, Dashti R, Laakso A, Elsharkawy A, Satopää J, Billon-Grand R, Canato B, Kivisaari R, Hernesniemi J.: Distal posterior inferior cerebellar artery aneurysms: Clinical features and outcome of 80 patients. World Neurosurgery, 2014 82(5):702 – 713

III Lehto H, Niemelä M, Kivisaari R, Laakso A, Jahromi BR, Hijazy F, Andrade H, Dashti R, Hernesniemi J: Intracranial vertebral artery aneurysms: Clinical features and outcome of 190 patients (World Neurosurgery, accepted)

The original publications here are reproduced here with the permission of the copyright holders.

9 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 7 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 8 30.3.2015 15.09 Abbreviations

ACA...... Anterior cerebral artery AICA...... Anterior inferior cerebellar artery AcomA .. Anterior communicating artery AVM...... Arteriovenous malformation AVF...... Ateriovenous fistula BA...... Basilar artery CCA...... Common carotid artery CI...... Confidence interval CN...... Cranial nerve CSF...... Cerebrospinal fluid CT...... Computed tomography CTA...... Computed tomography angiography DSA...... Digital subtraction angiography GOS...... Glasgow outcome scale H&H...... Hunt and Hess grade ICA...... Internal carotid artery ICH...... Intracerebral hemorrhage ISUIA..... International Study of Unruptured Intracranial Aneurysms IVH...... Intraventricular hemorrhage MCA...... Middle cerebral artery MRA...... Magnetic resonance angiography MRI...... Magnetic resonance imaging NA...... Not available OA...... Occipital artery OAG...... Occipital artery graft OR...... Odds ratio PCA...... Posterior cerebral artery PCKD...... Polycystic kidney disease PEG...... Percutaneous endoscopic gastrostomy PComA... Posterior communicating artery PICA...... Posterior inferior cerebellar artery RAG...... Radial artery graft SAH...... Subarachnoid hemorrhage SCA...... Superior cerebellar artery STA...... Superficial temporal artery UCAS...... Unruptured Cerebral Aneurysm Study of Japan VA...... Vertebral artery VBJ...... Vertebro-basilar junction 11 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 9 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 10 30.3.2015 15.09 Objective: Aneurysms of the vertebral artery (VA) and its branch posterior inferior cerebellar artery (PICA) are rare, comprising only about 1 to 3% of all intracranial aneurysms. The series published thus far on these lesions are small. We aim to describe the special anatomical and morphological features of these aneurysms compared to aneurysms in other locations, and to describe the variety of symptoms they cause. We describe their treatment and analyze the outcome. Additionally, we describe their anatomy imaged with computed tomography angiography.

Patients and methods: We reviewed retrospectively 9 709 consecutive patients with intracranial aneurysms treated in the Depart- ment of Neurosurgery at Helsinki University Central Hospital, Finland, between 1934 and 2011. The study population included 268 patients with 284 VA or PICA aneurysms or both. Follow-up data came from the Population Registry Centre (dates of death), Statistics Finland (causes of death), from written questionnaires to patients still alive, medical records of the Department of Neurosurgery, and for those deceased, medical records from all public health services.

Results: Among all the aneurysm patients, 5.1% had an aneurysm in the VA or PICA. Most aneurysms, 51%, were located at the VA–PICA junction. The proportion of fusiform aneurysms was 28%. Compared to patients with ruptured aneurysms at other locations, patients with a ruptured VA or PICA aneurysm were older and had a higher Fisher grade. Ruptured distal PICA aneurysms also re-bled more regularly. Compared to other Abstract ruptured aneurysms, ruptured VA and PICA aneurysms were smaller and more often fusiform. At least one VA or PICA aneurysm was treated in 209 (78%) patients. The most common technique for aneurysm occlusion was clipping, used in 107 aneurysms. Total occlusion of the aneurysm was achieved among saccular aneurysms in 90%, and among fusiform aneurysms in 61%. Within one year of aneurysm diagnosis, 26% of the patients were dead. Among those who survived a minimum one year and in whom the VA or PICA aneurysm received active treat- 13 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 11 30.3.2015 15.09 ment; those returning to an independent or their previous stage of life amounted to 92%.

Conclusion: In treatment of VA and PICA aneurysms, their special anatomical and morphological features are challenge. Despite this, and often severe hemorrhage, most patients surviving the initial stage make a good recovery. ❦

Vkirja_viite_255246_LEHTO_.indd 12 30.3.2015 15.09 Abstract 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 13 Vkirja_viite_255246_LEHTO_.indd 14 30.3.2015 15.09 Introduction

Intracranial aneurysms are acquired dilatations of cerebral arteries. Mostly they are saccular, pouch- like, and located at the branching point of an artery close to the skull base. Their prevalence in general population is 2 to 3% (232, 235). Almost all unruptured aneurysms are asymptomatic. When ruptured, they cause a subarachnoid hemorrhage (SAH), which manifests as sudden severe headache, nausea, and often also unconsciousness. The overall mortality from this disease is high, around 40% (158, 220). For previously diagnosed unruptured aneurysms, the annual rupture rate is around 1% (96). Risk factors for aneurysm rupture include smoking, female gender, and aneurysm size over 7 mm (111). Diagnosis of bleeding is made by CT or lumbal puncture; diagnosis of the aneurysm mostly by CTA or DSA. The posterior circulation consists of vertebral arteries, the basilar artery, and their branches. The vertebral arteries are paired and originate from the subclavian arteries. They ascend to traverse the skull through the foramen magnum, and join each other close to the pontomedullary junction to form the basilar artery. The posterior circulation comprises around 10% of all intracranial aneurysms (252). Compared to aneurysms in the anterior circulation, risk for rupture is also higher (244). Microsurgically, they are more difficult to access, and nowadays endovascular treatment is the preference in most centers. 17 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 15 30.3.2015 15.09 Figure 1 A typical PICA aneurysm

Special features of aneurysms arising study, we present 268 patients with 288 ver- from the vertebral artery, or from its branch tebral artery and PICA aneurysms. We aim posterior inferior cerebellar artery, are a high to report their incidence, features compared proportion of fusiform and dissecting aneu- to aneurysms at other locations, treatment, rysms, and many times a close relationship and outcome. Most aneurysms in this series to cranial nerves and to the brainstem. The were treated by microsurgery. ❦ course of the vertebral artery can be tortuous, and additionally, the course of PICA is the most variable among cerebral arteries. Figure 1.1 shows a typical PICA aneurysm. In addition to the series of Drake, Peerless, and Hernesniemi in 1966, other series on VA aneurysms are small. In this retrospective 18

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Cerebral artery aneurysms and subarachnoid hemorrhage Incidence and prevalence Overall prevalence of aneurysms in the general population is 2 to 3% (192, 232, 235). Overall, the incidence of aneurysmal subarachnoid hemorrhage is around 9/100 000 per year (43). The mean age of SAH patients has increased from 52 in the 1970s to 62 in 2000 (158).

Diagnostics Subarachnoid hemorrhage is practically always detectable on CT for a minimum of six hours after aneurysm rupture (16, 181). If needed, the diagnosis can be verified by lumbar puncture, which was also the method of diagnosis before the era of the CT scans. In aneurysm diagnostics, DSA has been the gold standard until recently but is now challenged by CTA (28, 238). Compared to DSA, CTA is less invasive, faster, cheaper, and has better availability; it makes reconstruction images is easier, and it visualizes better the bony structures in addition to the blood vessels (172, 233).

Risk factors The reported risk factors for aneurysm formation and growth are female gender and smoking (97). Risk factors for SAH include female gender, current smoking, aneurysm size over 7 mm, hypertension, excessive alcohol intake, and patient age inversely (52, 96, 111). Aneurysm growth during follow-up Review of is associated with rupture (97). Morphology and etiology the literature Morphologically, aneurysms are mostly divided into two categories: saccular and fusiform (non-saccular). By far most intracranial aneurysms are saccular. i.e. sac-like pouches mostly located in the bifurcation of an artery. Fusi- form aneurysms are spindle-shaped dilatations of an artery without clearly identifiable necks; their exact proportion is not known but has been estimated as less than 1% (12). Additionally, some authors further add to the categorization dissecting, dolichoectatic, serpentine, and atherosclerotic aneurysms. Dissecting aneurysms are morphologically mostly fusiform; a dissection of the vessel wall has led to its outward bulging. Dolichoec- 21 tasia is dilatation, elongation, and tortuosity Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 19 30.3.2015 15.09 of an artery, and when such an aneurysm ble throughout the vessel wall (59, 60). The contains thrombosis, it is called a serpen- degeneration may be related to impaired tine aneurysm. Atherosclerotic aneurysms function of the endothelium and high oxi- are morphologically fusiform, but show ath- dative stress, partly caused by intraluminal erosclerosis in their walls. thrombosis (60). All these terms overlap. The rare saccular- Similarly, fusiform aneurysms carry a de- shaped aneurysms located outside branch- fect in elastic lamina; in dissecting aneu- ing points of an artery are occasionally clas- rysms, the breakage is believed to be acute, sified as a separate group(148) . To distin- leading to intramural hemorrhage (49). In guish a non-saccular aneurysm from a nor- the chronic stage of fusiform aneurysms, mal vessel, Flemming et al., based on ra- beside disruption of the elastic lamina and diographic data, proposed dilatations great- intramural hemorrhage, neovascularization er than 1.5 times the normal vessel lumen occurs in the thickened intima and in the in- to be called aneurysms (57). Lately, Sacho et tramural thrombus formed (156). The new- al. used the same definition for a fusiform ly formed vessels also cause repetitive new aneurysm (200). To differentiate small fusi- hemorrhages within the vessel wall (156). form aneurysms from giant dolichoectatic ones, Flemming et al. further classified Genetics the non-saccular aneurysms into fusiform, A few, rare genetically inheritable diseas- dolichoectatic, and transitional groups: fu- es such as autosomal dominant polycystic siform aneurysms they defined as dilata- kidney disease may carry a higher incidence tion of a portion of an artery, dolichoectatic of intracranial aneurysms than in a normal as uniform dilatation of the whole artery or population (27). In general, studies on the several arteries, and transitional aneurysms genetics of patients with intracranial aneu- as dilatation of one or several arteries with rysms, show risk loci to be the same as in dilatation superimposed on one segment cardiovascular diseases (62), and SAH is pri- (56). Additionally, fusiform aneurysms are marily of non-genetic origin (113). occasionally divided into dissecting (acute) and chronic subgroups, with dissecting an- Treatment eurysms showing a classical “pearl-and- Acute treatment of aneurysmal SAH con- string” sign or double lumen in angiogra- sists of aneurysm occlusion to prevent re- phy and the chronic showing only a dilata- bleeding, prevention of delayed cerebral tion of the vessel (156). ischemia, standard medical management, and treatment of possible complications like Histology infections and hydrocephalus. Compared to the normal wall of a cerebral If the aneurysm is not occluded, a re- artery, the wall of a saccular aneurysm lacks bleeding occurs within the first 24 hours in elastic lamina and carries different degrees about 12% of all patients; most bleedings oc- of degenerative changes and inflammato- curring within six hours after the first ic- ry reactions (58, 106). The unruptured an- tus (219). After this, the risk remains at 1 eurysms’ wall have myointimal hyperplasia to 2% per day for next two weeks. After a and an organized thrombi, whereas the wall month, the risk decreases, but it remains matrix of a ruptured aneurysm is decellular- about 3% per year. Without aneurysm oc- ized and degenerated, there is ongoing in- clusion, mortality in SAH within a week is flammation, and lipid accumulation is visi- 40 to 45%, within a month 50 to 60%, within a year 65%, and within 5 years 65 to 70 % 22 (171). Because of the risk for rebleeding, an-

Vkirja_viite_255246_LEHTO_.indd 20 30.3.2015 15.09 Review of the literature

eurysm treatment is recommended within to the 1970s, in 1997, Hop et al. found a 15% first the 24 hours and at the latest within 72 decrease in case-fatality despite the higher hours after the first symptoms (41, 165, 220). mean age of SAH patients more recently. Antifibrinolytic drugs (tranexamic acid) re- Additionally, over the years, the proportion duce risk for rebleeding before aneurysm of patients who remain independent has in- treatment, but have no influence on poor creased by 1.5% per year (77). outcome or mortality (75, 193). In addition, those surviving beyond one The aneurysm is occluded either by mi- year after the bleeding have still excess mor- crosurgical or endovascular means. Micro- tality, mainly due to the higher risk of death neurosurgery consists mainly of clipping of especially in vascular events (83, 112, 243). A the aneurysm, but in rare cases involves trap- risk of recurrent SAH is within the first 10 ping or proximal occlusion with or without years is 3.2%, which is 22 times higher than bypass. Endovascular surgery consists main- the expected risk of SAH in general popula- ly of coil embolization of the aneurysm; in tion (242). The likelihood of de novo aneu- more complicated aneurysms, recent devel- rysm formation is 0.8% per year (97). opment has led to use of balloon- or stent-assisted embolization and flow-diverters. Preventive treatment Of patients surviving the initial hemor- Less than one-third of all unruptured an- rhage, cerebral ischemia occurs in about eurysms ever rupture, and identification 30%, mostly between days 4 and 10 (194). of those at risk is currently impossible. Be- Calcium antagonist (nimodipine) reduc- cause of the poor prognosis of aneurys- es both occurrence of the secondary isch- mal SAH patients, prophylactic treatment emia and risk for poor outcome (198). One of unruptured aneurysms is considered in recent study on preventive use of simvas- each case. The ongoing discussion conserns tatin showed no benefit(108) . which aneurysms and in which patients re- The figures on incidence of acute and quire treatment, and whether the aneurysm chronic hydrocephalus after subarachnoid should be treated by microsurgical or en- hemorrhage are variable: shunt-dependent dovascular means. Discussion is mainly hydrocephalus occurs in roughly 10% of focused on the International Study of Un- SAH patients (42). In a recent report, 33% ruptured Intracranial Aneurysms (ISUIA) of the patients later needed a shunt, with the published in 2003 in the Lancet (244). This predictive factors being poor clinical grade study includes 4 060 patients either being on admission, severe SAH, large ventricu- followed up or treated by surgery or endo- lar size before the aneurysm occlusion, and vascular procedures. Regardless of the high large amount of CSF drained within the first number of patients recruited, it has received week after bleeding (50). much criticism for selection bias, short follow-up, including posterior communicating Outcome artery aneurysms in the posterior circula- Despite treatment, the overall mortality of tion, and other matters. the patients with aneurysmal SAH is high, More recently, two other larger studies around 40% (158, 220). In a review of 2 424 have influenced this field: The Unruptured patients with outcome assessment ranging Cerebral Aneurysm Study of Japan (UCAS) from 1 to 12 months after SAH, 55% of the on the natural history of unruptured aneu- patients were independent, and 19% needed rysms, with 6 697 aneurysms studied with help in their daily activities (158). Compared a follow-up of 11 600 aneurysm-years, and development of the PHASES score, a score 23 aimed to predict aneurysm’s rupture risk. Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 21 30.3.2015 15.09 (63, 229) PHASES is based on systematic re- Compared to anterior circulation aneu- view of six earlier studies, an analysis in- rysms, one theory is that posterior circu- cluding 8 283 patients with a follow-up of lation aneurysms have a poorer natural 29 166 person-years (63). The study on the course. In ISUIA, the rupture rates for pos- natural history of aneurysms with the most terior circulation aneurysms ranged from extensive follow-up (median 21 years) and risk- 2.5% of those < 7 mm to 50% of giant aneu- factor analysis comes from Finland (96, 111). rysms, compared to 0% to 40% for the same Beside occlusion of the aneurysm, essen- size-groups in the anterior circulation (244). tial in preventive treatment are cessation of That study, however, grouped PComA aneu- smoking and treatment of hypertension (111). rysms as part of the posterior circulation aneurysms. In the UCAS study, with the excep- Posterior circulation aneurysms tion of large aneurysms, those located in the Definition posterior circulation were not more prone to Posterior circulation aneurysms consist of rupture than were aneurysms in the anterior aneurysms located in the posterior cerebral circulation (229). Both the UCAS and ISUIA artery, basilar artery, superior cerebellar ar- studies struggle, however, with rather short tery (SCA), anterior inferior cerebellar artery median follow-up times. Besides their pos- (AICA), vertebral artery, and the posterior in- sibly worse natural course, in SAH patients, ferior cerebellar artery (PICA). location of a ruptured aneurysm in the posterior circulation has been associated with Incidence poorer prognosis (195, 209). In the series of Yasargil, posterior circula- Anatomically, posterior circulation aneu- tion aneurysms accounted for 10% (252). rysms are located closer to the brainstem In a widely cited study from 1966, among and most of the cranial nerves, which chal- SAH patients with one aneurysm only, pos- lenges their surgical treatment. When anterior circulation aneurysms accounted for terior circulation aneurysms are treated via 5% (137). In a recent series on saccular aneu- pterional or lateral supraorbital craniotomy, rysms, those located in the posterior circu- or in the case of a pericallosal aneurysm, lation accounted for 9% (83). via an interhemispheric approach (38, 71, 127, 128), the complex anatomy of posterior cir- Location culation aneurysms demand a much wid- By far the most common location for the er range of craniotomies (226). Approaches posterior circulation aneurysm is the bas- used include far-lateral (73), suboccipital (47), ilar bifurcation (47, 82, 204, 233). In the se- pterional (252), subtemporal (47), transpetro- ries of Drake et al., basilar artery aneurysms sal (103) approaches and their variations. counted 51% (47). Treatment of unruptured posterior circulation aneurysms is also more prone to com- Special features compared to plications: based on ISUIA, in non-giant an- aneurysms in the anterior circulation terior circulation aneurysms, mortality and Classically, non-saccular aneurysms have morbidity is 1% and 2%, in non-giant poste- been thought to occur more frequently in rior circulation aneurysms 3% and 13%, in the posterior circulation (12). In the book of giant anterior circulation aneurysms 7% and Drake et al., of the posterior circulation an- 27%, and in giant posterior circulation aneu- eurysms, non-saccular aneurysms account- rysms 10% and 38% (244). ed for 225 (10%) (47). History of treatment 24 “I know of no successful outcome from oper-

Vkirja_viite_255246_LEHTO_.indd 22 30.3.2015 15.09 Review of the literature

Figure 2 The first known image of a VA aneurysm from 1829. ( reprinted

with

permission

from

www . jubiliotheque . upmc . fr )

ative attack upon an aneurysm of the posteri- ment of brachial and femoral cannulation, or cranial fossa, but for those upon the verte- vertebral angiographies become more rou- bral and posterior inferior cerebellar arteries, tine. Nowadays, the complication rate has which afford good exposure, cures will cer- been less than 0.5% (53). tainly come in time” (Walter Dandy 1944) (37) The first operations for posterior circulation aneurysms took place for presumed Worldwide tumors; the first was likely done by Cush- The first posterior circulation aneurysm ing in 1915. The first ligation of the cervical (basilar, autopsy finding) was descried by VA due to an intracranial aneurysm was by Blackall in 1813. The first illustration pre- Dandy in 1928 (37). The first successful di- served of a VA aneurysm is the one by Cru- rect treatment was reported by Schwartz on vilhier in 1829 (Fig. 2.21). November 6th, 1946: he trapped a ruptured The first VA angiography, done via injec- aneurysm of a an unnamed branch of the tion to a surgically exposed subclavian ar- basilar artery (210). The next successful sur- tery, was reported by Moniz in 1933 (149, 150). gery took place on January 23rd, 1947: Riz- Hugo Krauenbühl was the first to make the zoli et al. trapped and excised a PICA aneu- first posterior circulation aneurysm diagno- rysm (189). The first reported operation af- sis in an angiography in 1941; he used the ter aneurysm diagnosis by angiography was same method as Moniz (114). For many years, in 1956 by DeSaussure et al. (44), when they vertebral angiographies were done through trapped a PICA aneurysm. Drake, for his a direct puncture in the neck. After develop- part, operated on his first posterior circulation aneurysm in 1959; the patient with 25 a ruptured mid-basilar aneurysm clipped Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 23 30.3.2015 15.09 Figure 2.21 Patients with posterior circulation aneurysms diagnosed in Helsinki before 1980 14

0 1953 1960 1964 1968 1972 1976 1980

via a subtemporal approach made a good er developed by Serbinenko (213). Besides bal- recovery (47). According to Drake et al., be- loons, aneurysms were filled with an iron-par- fore 1960, 25 patients underwent surgery ticle suspension (Alksne, in 1969) and with for a ruptured basilar or vertebral artery an- isobytyl-2-cyanoacrylate (Sheptak, 1977), but eurysm; among them 10 were treated with the operations were done via a craniotomy or proximal vertebral artery occlusion. Among a burr hole (8). Additionally, Mullan et al. in these 25 patients, 4 died, but 16 suffered no 1965 described an electrically induced throm- adverse effect from the surgery(47) . bosis of an aneurysm: they punctured an an- Besides exovascular techniques, develop- eurysm though a craniotomy or a burr hole, ment of endovascular treatment is an impor- positioning a wire in the aneurysm and induc- tant part of the history of treating cerebral an- ing a current into it in order to produce throm- eurysms. Especially it involves posterior circu- bosis (153). Unfortunately, among the six aneu- lation aneurysms, as most are nowadays treat- rysms with angiographic follow-up, one aneu- ed by endovascular means. In 1964, Luessen- rysm showed 10% filling at two weeks; the oth- hop and Velasquez occluded a carotid aneu- ers were filling a minimum of 40%. In their rysm by endovascularly placing a silicone bal- report in 1974, they used the method also for loon into its neck (138); this method was lat- basilar aneurysms (154). In 1990, Dowd et. al. reported endovascular embolization of a PICA 26 aneurysm with platinum coils (45). Finally,

Vkirja_viite_255246_LEHTO_.indd 24 30.3.2015 15.09 Review of the literature

in 1991, Guglielmi reported his initial experi- The first attempt to embolize an aneu- ence with Guglielmi detachable coils. His in- rysm was done in Helsinki in 1991. The next vention allowed separation of the coil from year, came an attempt to embolize a posteri- the guide wire with an electric current at will, or circulation aneurysm. The first posterior which helps to control the coiling. The tech- circulation aneurysm was succesfully em- nique was further developed by Moret, who bolized in in 1994. The first balloon-occlu- introduced a “balloon-remodeling technique” sion of the ICA took place the same year as for wide-necked aneurysms reported in 1997 the first aneurysm embolization, 1991. The (151). Also in 1997, Higashida et al. published same year, an ICA aneurysm was filled with on treatment of a fusiform aneurysm of the a balloon. The VA was occluded for the first basilar artery with coiling through a stent (74). time with a balloon in 1997, and with coils Later, in 2008, Fiorella et al. published their in 2004. first experience in using a pipeline emboliza- Additionally, in 1976, ophthalmic aneu- tion device (55). rysm occlusion was attempted by filling it with some kind of filaments through a cra- Helsinki niotomy. Before 1980, 119 patients were diagnosed with a posterior circulation aneurysm (Fig- The vertebral artery and ure 2.21). The first diagnosis was made in the posterior inferior cerebellar artery 1953: a ruptured basilar bifurcation aneurysm was diagnosed at autopsy in a 57-year- Anatomy old woman. The first posterior circulation Vertebral artery aneurysm diagnosis based on angiography The paired vertebral arteries are the first and took place in 1958, when a PCA aneurysm largest arteries originating from the subcla- was diagnosed in the carotid angiography; vian arteries. Occasionally they can arise di- this patient refused surgery. In vertebral angiography, a posterior circulation aneurysm was found for the first time in 1960; the aneurysm was located in the basilar artery. Figure 2.22 This aneurysm was considered inoperable, Example of vertebral angiography from 1960 and the patient died from a re-bleeding. Fig- ure 2.22 shows a 1960 VA angiography. Before 1980, only 16 surgeries for posterior circulation aneurysm were performed in Helsinki. The first operation for a posterior circulation aneurysm was done in July 1961, when Tapio Törmä clipped a ruptured basilar bifurcation aneurysm. Unfortunate- ly the patient did not wake up from the surgery. In September 1961, Professor Gunnar af Björkesten wrapped a ruptured basilar bifurcation aneurysm. Postoperatively, this patient had hemiparesis, cranial nerve deficits, and memory deficits, but finally he recovered to an independent state. 27 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 25 30.3.2015 15.09 Figure 2.31 Extracranial VA

rectly from the aortic arch. Each vertebral The second VA segment (V2) runs in front artery is subdivided into four segments: the of the cervical nerve roots through the fora- first segment (V1) ascends to the C6 trans- men transversarium of the upper six vertebrae verse process, the second segment (V2) ex- to the axis. From the V2 segment originate the tends to the foramen of the transverse pro- cervicospinal branches for nutrition of the spi- cess of the atlas, the third segment (V3) up nal cord, nerve roots, and the vertebral bod- to the passage of the artery through the du- ies. In the narrowed corridor of the V2, an ex- ra, the fourth segment (V4) is intradural. ternal effect on the vertebral artery is possible The first VA segment (V1) ascends behind because of congenital anomalies, a narrowed the internal jugular veins between the mus- foramen transversarium, degeneration, os- culus longus colli and musculus scalenius teophytes, ligamentous hypertrophy, herniat- anterior. This segment is often affected by ed discs, or hypermobility of a cervical motion atherosclerotic wall transformation leading segment. Cervical luxation fractures can result to consecutive narrowing of inner vessel di- in a traumatic vertebral artery dissection or oc- ameter. clusion. The close relation of the vertebral artery to the cervical nerve roots exposes the ver- 28 tebral artery also to iatrogenic injuries.

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The third VA segment (V3) is closely re- In most cases, the left vertebral artery lated to the craniocervical junction and the is larger than the right, and a hypoplastic foramen magnum. After traversing the fo- vertebral artery is more often found on the ramen of C3 to reach the C2 tranverse pro- right side (104). Instead of terminating at the cess, the vertebral artery ascends laterally. A basilar artery, an atretic vertebral artery ter- vertically oriented segment traverses the C1 minates at the PICA, occipital artery, or spi- transverse process, after which a horizon- nal artery. Among the primitive arteries, the tal portion travels in a groove of the supe- proatlantal artery terminates at the vertebral rior surface of the posterior arch of the at- artery. las. Then V3 turns obliquely upward to reach the dura. The V3 segment is surrounded by Posterior inferior cerebellar artery the venous plexus, which is well perfused The PICA usually originates from the intra- by anastomoses between the deep cervical cranial segment (V4) of the vertebral artery. and epidural veins. The dural entrance lies However, an extra-cranial origin from the V3 just at the inferior-lateral side of the fora- segment is also possible. men magnum. A thick dura forms a tunnel There exists, as well, separate classifica- around 5 mm long around the vertebral ar- tions for segments of the PICA, the most tery. This tunnel also harbors the first cer- commonly used anatomy-oriented classifica- vical nerve, lying on the caudal surface of tion of Rhoton, and the more surgically ori- the VA, and the posterior spinal artery lying ented classification of Drake(47, 136). Rhoton posterior to the VA. Occasionally the dural divides the PICA into five segments: an an- tunnel is partially or even totally surround- terior medullary segment (1) extending up to ed by bone. During surgery, the V3 segment the most prominent point of the inferior ol- is important to obtain extra-cranial prox- ive. This segment may also be absent. A lat- imal control of the ipsilateral vertebral ar- eral medullary segment (2) continues up to tery. The segment can be affected by inju- the rootlets of CNs IX to XI. A tonsillomed- ries to the craniocervical junction. To protect ullary segment (3) extends until the mid-por- the VA from iatrogenic injuries, its identifi- tion of the PICA’s ascent along the medial cation by intraoperative Doppler ultrasound surface of the cerebellar tonsil. A telovelo- is very helpful. Anastomoses with the occip- tonsillar segment (4) terminates when the ital, ascending pharyngeal, and cervical ar- PICA exits to the suboccipital surface of the teries occur in the V3 segment. Commonly, cerebellum. The cortical segment (5) desig- the posterior spinal artery arises from the nates PICA’s terminal branches. V3 segment beside V4 segment. In varia- Drake divides the PICA into two seg- tions, an extra-dural origin of the PICA is ments: a proximal segment extending about also possible. one centimeter from its origin at the VA and The intracranial VA segment (V4) is subdi- a distal segment. vided into the lateral and anterior medullary The PICA shows several anatomical vari- segments, the division being at the preolivary ations. It may be absent or bihemispheric, sulcus. The anterior medullary segment lies supplying both hemispheres or with a bilat- on the clivus and terminates when the verte- eral vermian supply only, or its origin can bral arteries join each other to form the basilar be duplicate. The PICA can also originate artery usually near the pontomedullary junc- from the hypoglossal, proatlantal, or poste- tion. Intracranially, the vertebral artery gives rior meningeal artery. rise to the PICA and anterior spinal artery. A number of variations and anomalies of the PICA exist: some of them are listed in 29 Table 2.31. Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 27 30.3.2015 15.09 Table 2.31 Some reported anatomical PICA variations

Series (year) Variation Lesley (2008) (130) PICA fenestration Kumar (2012) (118) Trivelato (2011) (170) Double origin of PICA Pasco (2002) (176) Fine (1999) (54) Extracranial-extradural origin Uchino (2011) (230) PICA supplied by branch of ascending pharyngeal artery Okuno (1988) (166) Posterior meningeal artery rising form PICA Katsuno (2012) (101) Extracranial origin, anomalous with V3 Carlson (2012) (22) Bihemispheric PICA Manabe (1991) (143) PICA originating from the ICA Perot (2011) (180) Persistent trigeminal artery terminating in PICA Ali (2008) (7) Raphaeli (2009) (185) PICA supplied by trigeminal artery arising from a cavernous ICA Andoh (2001) (10) Persistent hypoglossal artery ending in PICA Kuruvilla (2011) (120) Middle meningeal artery originating from PICA Cho (2011) (30) Double origin with fenestration

Cranial nerves The nerves travel through the cerebellomed- The cranial nerves most frequently encoun- ullary cistern. After sending off a tympanic tered during surgery on vertebral artery an- branch, they exit the skull through the jug- eurysms are CN IX, (glossopahryngeal), X ular foramen. (vagus), and XI (accessory). They leave the In large VA aneurysms, CN VII (facial) medulla as a group of rootlets through the and VIII (vestibulocochlear) can also be en- postolivary sulcus, with the posterior olive countered, and if the aneurysm lies caudal- ventrally and inferior cerebellar peduncle ly, also CN XII (hypoglossal). Both CN VII dorsally. The cranial root forms CN IX, and and VIII merge from the pontomedullary three to five caudal rootlets the CN X and XI. junction, CN VII above CN VIII. They travel through the cerebellopontine cistern to 30 enter the internal acustic meatus. CN XII

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Figure. 2.32 VA, PICA, and cranial nerves photo

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emerges from the medulla in the preolivary The other controversy involves categori- sulcus, i.e. with the pyramid anteriorly and zation of PICA aneurysms. A “PICA aneu- inferior olive posteriorly. The nerve consists rysm” typically refers to an aneurysm either of 10 to 15 small rootlets, which converge into at the VA–PICA junction or more distally two bundles to enter the hypoglossal canal. in the PICA. The term “proximal PICA aneurysm” is used either for an aneurysm at Controversies in nomenclature the VA–PICA junction only (47), or also for The present literature displays a few contro- those arising from the anterior medullary versies regarding nomenclature related to segment of the PICA (24), or any medullary VA and PICA aneurysms. First, the defini- segment of the PICA (133, 177). Aneurysms at tion of the PICA is diverse: it is defined ei- the PICA outside VA–PICA junction are al- ther as an artery originating from the VA to so called “true PICA aneurysms” (258). supply the cerebellum (136, 252), or as an artery originating from the VA or the basilar Aneurysms artery to supply the posterior inferior part of Incidence the cerebellum (251). Due to high variation in Probably due to their rarity, reports on inci- the area supplied by the PICA, we defined dence of VA and PICA aneurysms in a non- as PICA the vessel originating from the VA selected series are scarce. In the series of Ya- to supply the cerebellum. maura et al., the prevalence of VA and PI- CA aneurysms among posterior circulation 31 aneurysms was 32% (250). In a cooperative Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 29 30.3.2015 15.09 study from Japan, among ruptured saccu- PICA aneurysms also had a posterior fos- lar aneurysms, those located in the VA or sa AVM, which could at least in part ex- PICA accounted for 1.9%; among posterior plain the high number of distal PICA an- circulation aneurysms they accounted for eurysms. 39% (253). In the vertebrobasilar aneurysm In previous series, location of distal PICA series of Drake et al., VA and PICA aneu- aneurysms have been mainly reported rysms accounted for 12.5% (47). In the Co- according to the classification of Rhoton(15, operative study from 1966, among SAH pa- 78, 91, 92, 131, 167, 227). The reported distribu- tients with a single aneurysm only, those lo- tion of aneurysms has been slightly vari- cating in the VA or PICA numbered 1.3% able: Horiuchi et al. in their series of 27 (137). In a Finnish study on saccular aneu- distal PICA aneurysms reported the most rysms, the incidence of VA and PICA aneu- common location to be the telovelotonsillar rysms was 2.4% (82). segment (30% of aneurysms), followed by Mere PICA aneurysms are believed to the lateral medullary segment (26%) (78). comprise 0.5 to 3%. Among all treated an- Tokimura et al. found 9 (30%) aneurysms eurysms, Peluso et al. reported 2.8% to be in the lateral medullary segment, and as located in the PICA (177). In 2013, Baciga- the next common location, 7 (23%) aneu- luppi et al. reported in 621 patients the inci- rysms in the tonsillomedullary segment dence of PICA aneurysms as being 3.7% (15). (227). Lewis et al. reported the most com- In the series from Kuopio, Finland, at the mon location of distal PICA aneurysm to junction of PICA were located 1.9% of aneu- be the cortical segment; they included in rysms (82). The incidence of distal PICA an- their series of 20 patients 6 with an AVM eurysms is low, 0.56% of all aneurysms ac- (131). In the series of Orakcioglu, the two cording to a report by Ishikawa et al. in 1990 most common locations, with an equal dis- (91) and 0.86% in a report by Tokimura et al. tribution of 33%, were the anterior medul- in 2011 (227). lary segment and telovelotonsillar segment (167). With the exception of the report of Location Lewis et al., the larger series report medul- Most VA and PICA aneurysms are located lary segments as being the most common at the junction of these vessels (47, 82, 250). location for a distal PICA aneurysm (78, 167, In the series of Drake et al., they account- 190, 227). ed for 69% (47). Altogether in their series, the number of aneurysms located in the Morphology and etiology proximal VA was 8 (3%), the VA–PICA In the VA, saccular aneurysms, located at junction 168 (69%), distal VA 41 (17%), and the junction of the PICA, are by far most distal PICA 26 (11%). Bertalanffy et al. in common. The proportion of fusiform an- 1988 reported their experience with the VA eurysm ranges from 13 to 26%, and dis- and distal PICA aneurysms: in the prox- secting 7 to 28% (11, 19, 47, 250). Dolicho- imal VA were located 5 (21%), VA–PICA ectasias many times reach from the ver- junction 7 (29%), distal VA 3 (13%), and tebral artery to involve also the basilar ar- in the distal PICA 9 (38%). In this series, tery (12, 57, 187, 245); the incidence of those distribution of the PICA aneurysm is ex- located in the vertebral artery alone is un- ceptional, with distal PICA aneurysms known. Serpentine aneurysms are mostly outnumbering aneurysms at the origin of in case-reports (169, 224, 234). In the distal PICA. However, three patients with distal PICA alone, fusiform aneurysms account for 7 to 41% and dissecting 0 to 41% (78, 32 131, 167, 227).

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Table 2.32 Larger surgical series conserning VA and distal PICA aneurysms

Series (Year) Year No. of aneurysms Notes Series (Year) 2008 6 Dissecting distal PICA aneurysms only Horiuchi (78) 2007 24 Distal PICA aneurysms only Al-khayat (3) 2005 52 Study on lower cranial nerve palsies Liew (133) 2004 13 Study on lower cranial nerve palsies D’Ambrosio (35) 2004 20 Nussbaum (161) 2003 7 Fusiform distal PICA aneurysms only Lewis (131) 2002 20 Distal PICA aneurysms only Matsushima (145) 2001 8 Horowitz (79) 1998 38 Bertalanffy (19) 1998 27 Sano (207) 1997 45 Dissecting aneurysms Andoh (11) 1992 38 Yamaura (249) 1990 24 Dissecting aneurysms Ishikawa (90) 1990 12 Distal PICA aneurysms only Yamaura (250) 1988 86 Gacs (61) 1983 16

Symptoms 47, 133, 224, 254), lateral medullary syndrome As with all intracranial aneurysms, most (86), bulbar palsy (1, 17, 47, 64, 85, 133, 144, 237), VA and PICA aneurysms are found as a re- gaze palsy (47, 129, 177, 183, 240), nystagmus sult of subarachnoid hemorrhage (11, 250). Yet (19, 84, 216, 224, 240), impaired hearing (47, the close location of the cranial nerves and 129, 237, 254), facial nerve palsy or hemifacial the brainstem occasionally causes the aneu- spasm (17, 47, 110, 208, 231, 237), or trigeminal rysm to manifest as a cranial nerve deficit symptoms (12, 47, 152). These symptoms are or as symptoms caused by brainstem com- occasionally also caused by compression of pression (12, 19, 47, 139, 179). Symptoms caused the hemorrhage upon the neural structures by mass effect include ataxia (47, 64, 79, 85, (47, 139). Additionally, a giant aneurysm can 131, 224, 237, 239), sensory loss or paresthesias cause obstructive hydrocephalus (47). (47, 183), hemi-, para-, or tetraparesis (2, 12, 13, Besides SAH and symptoms caused by compression, VA dissecting aneurysms are associated with cerebellar and brainstem 33 ischemia (12, 87, 98, 99, 140, 188, 250). Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 31 30.3.2015 15.09 Table 2.33 Some reported approaches to VA and distal PICA aneurysms

Approach Reference Suboccipital 47, 68, 80 Midline suboccipital subtonsillar 70 Midline (medial) suboccipital 72, 125, 196, 203 Paramedian suboccipital 252 Combined lateral and medial suboccipital 20 Suboccipital transcondylar 103 Lateral suboccipital 11, 19, 72, 203, 250 Lateral suboccipital and partial condylectomy without laminectomy 255 Far-lateral 73, 115, 122 Far-lateral suboccipital 26, 35, 164 Far-lateral supracondylar 241 Far-lateral paracondylar 241 Far-lateral with partial condylar resection 100 Far-lateral approach with resection of occipital condyle 157 Far-lateral transcondylar 19, 40, 46, 145, 241 Far-lateral transcondylar transtubercular 218 Transcondylar fossa (supracondylar transjugular tubercle) 145 Extreme lateral transcondylar 14, 191 Extreme-lateral inferior transtubercular 39, 202 Extreme lateral, transcondylar, transjugular 211 Contralateral far-lateral 21 Presigmoid transpetrosal 103 Retromastoid 68 Subtemporal 121 Pterional 121 Transfacial transclival 26 Minimally invasive supracondylar (MIST) 197 34

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Figure 2.33 nerves many times in close proximity to the Lateral sucboccipital craniotomy aneurysm. Another challenge is the complete and stable occlusion of fusiform (dissecting) aneurysms. As one approach, most surgeons favor the far-lateral approach described especially by Heros (72) (Table 2.33). Its extensions have been divided according to their relation to the occipital condyle, i.e. transcondylar, paracondylar, and supracondylar (231). Another common approach is the lateral suboccipital (Figure 2.33) or the retrosigmoid approach, which consists of less bony opening than with the far-lateral approach. The suboccipital approach was favored by Drake et al. (47). In our department, Professor Juha Hernesniemi uses a small retrosigmoid craniotomy for most VA and PICA aneurysms. The prerequisite for this approach is location of the lesion a minimal 10 mm above the foramen magnum. Aneurysms located below this line require a more lateral approach. In- stead of the classic far-lateral approach, the choice is an approach “lateral enough.” In Treatment this, the foramen magnum is opened, but In VA and PICA aneurysms, the challeng- in most cases C1 is left intact. When needed, es caused by location, variable morpholo- removing part of C1 or minimal drilling of gy, and etiology have led to a wide range the occipital condyle extends the approach. of techniques for their occlusion. This can Drilling the whole condyle as in the trans- be seen also in the studies published after condylar approach, drilling of the jugular 2000, with methods including clipping (35, process as in the paracondylar approach, or 204), wrapping (204), surgical proximal oc- drilling of the jugular tubercle as in the su- clusion or trapping in possible combina- pracondylar approach have been unneces- tion with a bypass (35, 87, 204), selective coil- sary. For aneurysms in the cortical branching (177), internal trapping (119), stent-assist- es of the PICA close to the midline, the ap- ed coiling (31), or mere stenting or use of a proach is a median or paramedian suboc- flow-diverter (25, 256), proximal occlusion cipital. The small craniotomies require good with coils or balloon (177), and endovascu- neuroanesthesia and spinal drainage to gain lar vessel occlusion combined with bypass maximal space for dissection. surgery (65). Even if the primary method used for surgical aneurysm occlusion is clipping, espe- Microneurosurgery cially in fusiform (dissecting) or giant an- In Table 2.32, see surgical series on VA and eurysms clipping may be impossible. When PICA aneurysms. Surgical treatment is treated surgically, these cases may require mainly challenged by location of the cranial VA or PICA occlusion. A non-dominant VA distal to the PICA can in most cases be oc- 35 cluded safely. It is assumed that distal PI- Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 33 30.3.2015 15.09 Figure 2.34 Clipping of a PICA aneurysm photo

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Vkirja_viite_255246_LEHTO_.indd 34 30.3.2015 15.09 Review of the literature

CA can also be occluded safely distal to the Outcome medullary segments, as no perforators to Radiological the brainstem typically arise after this point In the surgical series of Drake et al. (221 an- (136). This, however, has turned out to be eurysms), total occlusion of the VA and dis- somewhat unreliable (92). When in doubt tal PICA aneurysms was achieved in 86% as to the safety of occluding VA or PICA, and a neck remnant was found in only 4% some authors advocate using a balloon oc- (47). That series also included 59 aneurysms clusion test, while others limit its use to the treated with Hunterian ligation and 7 aneu- anterior circulation (215, 217, 223). If the pa- rysms treated with wrapping. In the more tient fails the balloon occlusion test, or oth- recent series of Sanai et al., among 59 aneu- erwise needs flow augmentation, the most rysms, all but one clipped PICA aneurysm commonly used are or OA–PICA bypasses and three wrapped aneurysms were total- (9, 34, 123, 129, 161, 212). The other possibilities ly occluded, giving a total occlusion rate of include re-anastomosis of the PICA (64, 123, 93% (204). 161), (re-)implantation of the PICA to the VA In a recent endovascular series of 76 prox- (17, 123, 162, 163) or to the AICA (51, 126), AICA– imal and distal PICA aneurysms, complete PICA side-to-side anastomosis (51) VA–RAG occlusion was achieved in 63% (24). In a se- / OAG / vein graft–VA (51, 116, 123), CCA–RAG ries of Endo et al. on internal trapping of 38 / vein graft–PICA (32, 212), PICA–STA–VA ruptured VA dissecting aneurysms, after pri- bypasses (64 – 66). mary total occlusion 5 (21%) aneurysms re- canalized (48). In a series of Lv et al. on 22 Endovascular treatment dissecting aneurysms of VA and PICA treat- Endovascular treatment has gained popular- ed with various endovascular methods, 6 ity for VA and also in PICA aneurysms (Ta- (27%) aneurysms were totally occluded (140). ble 2.33). With the advantage of no cranial nerve manipulation, endovascular treatment Clinical still is, however, challenged by attempts to In good-grade patients, the outcome of treat- keep the PICA open, and to achieve com- ment is generally favorable. In the series of plete occlusion of the aneurysm. The small Drake et al., among the 181 good-grade (Bot- caliber and tortuous course of the PICA chal- terel classification grades 0 to 2) patients lenge treatment of distal PICA aneurysms in with non-giant aneurysms, only 2 poor out- particular. In recent years, the number of pa- comes and 4 deaths occurred (47). In series pers on endovascular treatment of VA and of Yamaura et al. on VA aneurysms, GOS distal PICA aneurysms, dealing with the 4 to 5 recoveries occurred in 64 (94%) of challenges and advantages of endovascu- surgically treated patients (250). In their re- lar treatment has been growing (24, 33, 225, cent surgical series, GOS 4 to 5 occurred in 228). Besides selective embolization, inter- 42 (76%) (205), 47 (90%) (3), and 14 (94%) nal trapping has been useful, especially in patients (35). Morbidity from surgery is ma- distal PICA (15, 24, 92, 134, 168) and dissecting ny times related to cranial nerve deficit: up VA aneurysms (48, 105, 124, 178, 222). To avoid to 48% of patients suffer from lower crani- a vessel occlusion, use of stent-assisted coil- al nerve palsies (3, 19, 79, 250). In a study on ing (95, 107, 155, 186, 201), mere stenting (95, 175, 52 patients with such postoperative palsies, 186, 201, 256, 257), or lately also flow diverters within 6 months 76% recovered (3). Even has evolved (6, 25, 182, 184, 199, 236). better outcomes have been reported: in the series of Yamaura, only one patient of eight with lower cranial nerve palsies was left with 37 a hoarse voice (250). Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 35 30.3.2015 15.09 Figure 2.33 Recent series on VA and PICA aneurysms Treatment Endovascular Endovascular Endovascular Endovascular Endovascular Endovascular Endovascular Endovascular and surgical Endovascular Endovascular Endovascular Endovascular and surgical Endovascular and surgical Endovascular and surgical Endovascular Endovascular Endovascular and surgical Endovascular Endovascular 7 7 8 9 9 9 15 12 14 23 38 10 10 72 28 76 26 20 111 No. of patients Chen et al. (2013) (29) Dabus et al. (2013) (36) Ishihara et al. (2013) (89) et. al. (2013) (228) Trivelato Chalouhi et al. (2013) (24) et al. (2013) (246) Wu Cho et al. (2013) (31) Bacigaluppi et al. 2013 (15) Endo et al. (48) Suma et al. (2013) (225) Ioannides et al. (2013) (88) Lin et al. (2012) (135) Su et al. (2011) (222) Hong et al. (2011) (76) Kim et al. (2011) (105) Shin et al. (2011) (214) et al. (2011) (227) Tokimura et al. (2010) (139) Lv Sadato et al. (2010) (201)

In their series including both endovas- patients with ruptured VA dissection, a cular and surgical treatment of the aneu- modified Rankin Score of 0 to 2 was report- rysms, Hong et al. reported a GOS 5 to 4 ed in 61% (23 patients) (48). Among prox- outcome in 65% of patients with ruptured imal and distal PICA aneurysms in SAH PICA aneurysms (76). In a series on distal patients, GOS 4 to 5 recovery was noted in PICA aneurysms, of 24 patients with a rup- 77% (24). In another study on proximal PI- tured aneurysm, 19 (79%) recovered to GOS CA aneurysms, GOS 4 to 5 occurred in 68% 4 or 5 (227). (177). In a study on patients with lower crani- In one recent endovascular series, among al nerve palsy caused by a PICA aneurysm, the palsy recovered totally in 6 months in 9 38 (75%) (139). ❦

Vkirja_viite_255246_LEHTO_.indd 36 30.3.2015 15.09 Review of the literature Endovascular Endovascular and surgical Endovascular Endovascular Endovascular Endovascular Endovascular Endovascular and surgical Endovascular Endovascular Endovascular Endovascular Endovascular Endovascular and surgical Endovascular Surgical Endovascular and surgical 5 6 9 6 11 15 15 31 12 25 52 23 16 22 28 24 46 Lee et al. (2010) (124) Nourbakhsh et al. (2010) (159) et al. (2010) (140) Lv et al. (2010) (141) Lv Jeon et al. (2009) (94) He et al. (2009) (69) Isokangas et al. (2008) (92) Li et al. 2008 (132) et al. (2008) (23) Cellerini Peluso et al. (2008) (177) Kudo et al. (2007) (117) Mericle et al. (2006) (146) Maimon et al. (2006) (142) Orakciolgu et al. (2005) (167) Albuquerque et al. (2005) (4) Al-khayat et al. (2005) (3) Sandalcioglu et al. (2005) (206)

39 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 37 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 38 30.3.2015 15.09 Aims of the study

1. To describe the anatomy of PICA aneurysms as diagnosed by CTA (Study I)

2. To clarify the special features of intracranial VA and distal PICA aneurysms (Studies II and III)

3. To describe the treatment of VA and distal PICA aneurysms, and analyze the outcome of the treatment (Studies II and III) ❦

41 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 39 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 40 30.3.2015 15.09 Patients We reviewed retrospectively 9 709 consecutive patients with intracranial aneurysms treated in the Department of Neurosurgery at Helsinki University Central Hospital, Finland, between 1934 and 2011. We excluded, to ensure a population-based material, those referred from abroad. We also excluded all vertebro-basilar junction aneurysms or aneurysms extending to the basilar artery.The study population thus included 268 patients with 284 VA or PICA aneurysms or with both.

Study I (Seventy aneurysms of the posterior inferior cerebellar artery: anatomical features and value of computed tomography angiography in microneurosurgery) included 70 patients with VA–PI- CA junction aneurysms imaged by CTA.

Study II (Intracranial vertebral artery aneurysms: clinical features and outcome of 190 patients) included 190 patients with 193 VA aneurysms, including aneurysms at VA–PICA junction.

Study III (Distal posterior inferior cerebellar artery aneurysms: Clinical features and outcome of 80 patients) included 80 patients with 91 aneurysms in distal PICA.

Aneurysms were identified either by CTA, DSA, conventional angiography, or by MRA, or at autopsy, or they were merely surgical findings. CT, lumbar puncture, or autopsy diagnosed SAH. A suspected incidental aneurysm was considered earlier ruptured if a clear surgical finding of a former rupture was evident (visual- ized rupture site in the aneurysm with hemosiderin next to it, with no other source of hemorrhage). In cases of multiple aneurysms, the site of rupture was decided based on CT findings, size and irregularity of the aneurysm, or findings in surgery or at an autopsy or both. In cases of AVM and associated aneurysm, the rupture site was diagnosed based on findings in CT, surgery, and possibly at autopsy. Patients’ neurological status was assessed Patients and on the Hunt and Hess scale (H&H) without the correction for general disease (81). We compared patients with a ruptured methods VA and PICA aneurysm to those with a ruptured aneurysm elsewhere (age, gender, aneurysm size and morphology, number of aneurysms, Fisher grade, occurrence of IVH or ICH, rebleeding rate, and H&H). 43 We used for comparison all other patients Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 41 30.3.2015 15.09 treated for ruptured intracranial artery an- Table 4.21 eurysm in the Department of Neurosurgery, Imaging methods used for aneurysm diagnostics Helsinki, Finland, from 1980 to 2009. The patients treated before the era of CT scan- Angiography No. of aneurysms ning and microsurgery, i.e. before 1980, were excluded from this part of the study. DSA only 116 CTA only 74 Data and analysis MRA only 2 Radiological data DSA and CTA 55 The radiological images were re-reviewed by a neurosurgeon-radiologist (Riku Kivisaari). DSA and MRA 5 Digital archiving started in 1999, and the DSA, CTA and MRA 9 images were reviewed with AGFA Impax CTA and MRA 11 (version 5.3, Agfa, Mortsel, Belgium). Imag- ing studies from 1989 onwards were avail- CTA, computed tomography angiography; DSA, able for review. In cases in which images digital substraction angiography; MRA, magnetic were unavailable or their quality was poor resonance angiography (n = 44, 16%), the data came from radiological and surgical reports. The first CT-scanner came to Töölö Hos- pital in 1980. Since acquiring the CTA pro- gram, the examinations were preformed for screening, in patients with iodine aller- with a 4-slice scanner until 2007 (GE Light- gy, and MRI together with MRA when study soeed QX/I; GE Medical Systems, Milwau- (partially) thrombosed aneurysms. Addition- kee, WI, USA) and later with a 32-slice scan- ally, patients are also admitted to our clinic ner (GE LightSpeedPro 32) or 64-slice scan- with their aneurysms diagnosed by MRA. ner (GE LightSpeed VCT Advantage). Table 4.21 shows the different imaging SAH was diagnosed either by CT (192 pa- methods used for VA and PICA aneurysm tients) or lumbal puncture (31 patients). In diagnostics. One patient had no preopera- an additional three patients the aneurysm tive angiography, as the aneurysm was ini- was incidentally found, but during surgery tially wrongly diagnosed as recurrent he- hemosiderin around the aneurysm was a mangioblastoma. Five aneurysms were in- sign of earlier bleeding. traoperative findings: preoperatively, DSA For aneurysm diagnostics, conventional was performed in three, CTA in one, and cut film angiography was used in our clin- both DSA and CTA in one case. Two of ic until 1991. After this, DSA was the on- these aneurysms were thrombosed, and ly method until 1995 when CTA was intro- three were 2-mm aneurysms, found during duced. Since 2000, CTA has been the pri- an operation performed for another VA or mary aneurysm-diagnostic method for SAH PICA aneurysm. At autopsy 14 aneurysms patients, and is also always performed be- were diagnosed: 11 had no kind of angiogra- fore aneurysm surgery. Nowadays, we per- phy, in 3 aneurysms DSA had been negative. form DSA if endovascular surgery is consid- In each aneurysm we measured the max- ered, if CTA remains negative, or if a suspi- imal width and length of the sac, and the cion arises of a small aneurysm, or in case of neck diameter (Fig 4.21). Maximal diame- a need to study flow dynamics. We use MRA ter of both saccular and fusiform aneurysms was considered the largest measurement in 44 any direction.

Vkirja_viite_255246_LEHTO_.indd 42 30.3.2015 15.09 Patients and methods

For the anatomical study based on CTA ent health status. For those who did not re- (Study I), all the CTAs were reanalyzed. spond, we obtained the follow-up data only We measured the relationship of the aneu- from the department of neurosurgery. For rysm to the skull base (distances from fora- those deceased, we used medical records men magnum, midline, closest bony struc- from all public health services. ture, clivus, and relation to hypoglossal canal and jugular tubercle). Additionally, we Statistical analysis measured the size of the jugular tubercle in We performed the data analysis by IBM three dimensions. We recorded anatomical SPSS Statistics, version 20.0.0 for Mac (a variations in the VA, cerebellar arteries, bas- commercial statistical software). To com- ilar artery, and also possible persistent fetal pare groups, we used Pearson’s x² or Fish- anastomoses, additional aneurysms, AVM, er’s exact test for categorial variables, and and AVF. We measured size of the PICA at the Mann-Whitney U-test for continuous its origin; if the PICA could not be visual- variables. We considered probability val- ized in CTA, it was considered hypoplastic. ue < 0.05 statistically significant. We ana- The VA we considered hypoplastic, if its di- lyzed the risk factors for death at one year ameter was equal to or less than 2 mm at after treatment of ruptured VA or PICA an- the level of the foramen magnum (173). If eurysm. In univariate analysis we included no VA was visible distal to PICA, it was con- age, gender, Fisher grade, size and morphol- sidered atretic. ogy of the aneurysm, possible re-bleeding, shunt-dependent hydrocephalus, and H&H Follow-up data grade in good-grade (H&H 1 to 3) and poor- We followed up the patients until death or grade (H&H 4 and 5) grade groups, as well the end of 2011. The Population Registry as decade of treatment. To calculate odds Centre, comprising all Finnish residents, ratios (ORs) and 95% confidence intervals provided the vital status of the patients on (CIs) of independent factors associated with December 31, 2011, as well as possible date of one-year case fatality, we used uncondition- death. The causes of death came from Sta- al binary logistic regression analysis. To a tistics Finland (http://www.stat.fi/index_ stepwise forward elimination procedure, en.html). To those still alive we sent a writ- the selected variables were added on the ba- ten questionnaire concerning their pres- sis of their probability values. ❦

Figure 4.21 Measurement of saccular (left side) and fusiform (right side) aneurysms. L = length, W = width, N = neck

W W L L

45 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 43 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 44 30.3.2015 15.09 Table 5.21. Patient characteristics (n = 70)

Gender No. (%) Female 47 (67) Male 23 (33) Results Age median (range) All 59.5 (29 – 85) Presentation No. (%) SAH from 42 (60) PICA aneurysm Incidence of vertebral and posterior SAH from another inferior cerebellar artery aneu- 11 (16) rysms aneurysm After 2000, all aneurysm patients treated in Incidental 13 (19) our clinic have been investigated with cere- Screening 1 (1) bral CTA or MCA, or in rare cases only autopsied. Among these patients, those diag- Mass lesion 2 (3) nosed with a VA or PICA aneurysm or both Total number of No. (%) accounted for 5.1%. Of those with aneurys- aneurysms per patient mal SAH, the rupture site was in the VA or 1 38 (54) PICA in 3.9%. Of all aneurysms, 3.7% were 2 10 (14) located in the VA or PICA. 3 17 (3) Anatomy of aneurysms at junction 4 2 (3) of the vertebral artery and the posterior 5 1 (1) inferior cerebellar artery 6 1 (1) Patients and aneurysms In 70 patients the saccular aneurysm at the 7 1 (1) VA–PICA junction was diagnosed by CTA, each had one PICA aneurysm (Table 5.21). PICA, posterior inferior cerebellar artery; Multiple aneurysms were diagnosed in 32 SAH, subarachnoid hemorrhage patients, with 17 patients suffering from SAH from an aneurysm at another location. Two PICA aneurysms were diagnosed due to mass effect. The most common associated aneurysm was that of MCA (Table 5.22). No patient had multiple aneurysms in the VA or PICA; one had an occipital AVM.

PICA aneurysms Location Of the 68 postPICA aneurysms and 2 prePI- CA aneurysms (Figure 5.21), most (61%) 47 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 45 30.3.2015 15.09 Table 5.22. Table 5.23 Associated vascular lesions Distance from PICA aneurysm to adjacent anatomical structures No. of No. of patients lesions Median (m) Range (mm) Aneurysm Distance from ICA 11 15 the foramen 16.5 -1.0 – 31.0a magnum MCA 23 34 Distance from ACA 10 10 6.0 -7.5 – 14.0b the midline BA 5 8 Distance from 11.0 3.0 – 33.0 AVM 1 1 the clivus Distance from ACA, anterior cerebral artery; AVM, arteriovenous 4.0 1.0 – 15.0 malformation; BA, basilar artery; ICA, internal the bone carotid artery; MCA, middle cerebral artery a Negative figure located below the foramen magnum. b Negative figure located on the contralateral site of the skull compared to parent artery origin.

were on the left side. Most were within 10 10 (14%). Five aneurysms (7%) were par- mm from the midline, at a distance ranging tially thrombosed: two were medium- from 8 mm contralateral to 14 mm to ipsi- sized (7–14 mm), two large (15-24 mm), lateral of the side of the parent artery (Table and one giant (> 24 mm). 5.23). On the contralateral side of the skull were four aneurysms (Figure 5.22). In re- Variations of VA and PICA lation to the foramen magnum, one aneu- The left VA was larger than the right (p = rysm was located below it (Fig. 5.23), within 0.002); the median diameter of the left VA 10 mm above it were 15 (22%), from 11 to 20 was 2.8 mm (range 0-4.8) and of the right mm were 23 (47%) and over 21 mm above the VA 2.1 mm (range 0-4.1). Both hypoplastic foramen were 20 (29 %). Table 5.24 presents and atretic VAs were more frequent on the location of aneurysms in relation to different right side, as was the hypoplastic PICA (Ta- skull base structures. To the skull base were ble 5.26). Hypoplastic VA on both sides was attached 11 (16%) aneurysms. diagnosed in two patients; an additional two patients had the right VA thrombosed. Of Morphology the aneurysms, 89% were located on the Maximum median diameter of aneu- dominant VA. One patient had an aneurysm rysms was 5 mm (Table 5.25). Small an- on the side of a hypoplastic PICA. Two PI- eurysms, with a maximal size of 6 mm, CAs were of extracranial origin. numbered 48 (69%). Only one aneurysm was giant. Calcifications were present in Jugular tubercle Of the 70 aneurysms, the level of the jug- 48 ular tubercle was the location of 39 (56%).

Vkirja_viite_255246_LEHTO_.indd 46 30.3.2015 15.09 Results 30.3.2015 15.09 Figure 5.22 Figure 5.22 Left PICA aneurysm on the right side of the posterior fossa as compared to origin of the parent artery 49 1 (1) 5 (7) 15 (21) 10 (14) 39 (56) No. of aneurysms (%) Aneurysms of the vertebral and posterior inferior cerebellar arteries Extracranial Below the hypoglossal canal At the jugular tubercle Above the jugular tubercle At the hypoglossal canal Table 5.24. 5.24. Table Aneurysm in relation to skull base PrePICA (left) and postPICA (right) aneurysms and postPICA (right) PrePICA (left) Figure 5.21 Figure 5.21 Vkirja_viite_255246_LEHTO_.indd 47 Figure 5.23 Figure 5.24 Aneurysm located extracranially A left jugular tubercle

Table 5.25. Sizes of VA – PICA junction aneurysms

Ruptured Unruptured Total Number of aneurysms 42 28 70 Measurements median (range) median (range) median (range) Maximal size (mm) 6 (2 – 20) 4 (2 – 27) 5 (2 – 27) Length (mm) 6 (1 – 20) 4 (1 – 27) 5 (1 – 27) Width (mm) 4 (2 – 13) 3 (2 – 20) 4 (2 – 20) Neck (mm) 3 (2 – 6) 3 (1 – 8) 3 (1 – 8) Neck-to-width 0.7 (0.3 – 1.0) 0.8 (0.2 – 1.0) 0.7 (0.2 – 1.0) Size distribution No. No. No. < 7 mm 28 20 48 7 – 14 mm 13 5 18 15 – 24 mm 1 2 3 > 24 mm - 1 1 50

Vkirja_viite_255246_LEHTO_.indd 48 30.3.2015 15.09 Results 30.3.2015 15.09 1960 1970 1980 1990 2000 Figure 5.31 Figure 5.31 Decade of admission Table 5.31 summarizes patient characteris- 5.31 summarizes patient Table The 268 patients harbored altogether 445 0 75 25 50 (28%). Besides VA or PICA aneurysms, an- (28%). Besides VA eurysms elsewhere in the posterior circula- patients had tion occurred in 21 (8%). Nine additional aneurysms diagnosed later (Table aneurysm was diagnosed in 4.2%. Among aneurysm was diagnosed in 4.2%. Among and PICA aneurysms ac- all aneurysms VA an- counted for 3.2% and among ruptured eurysms 5.3%. tics, revealing a slight female predominance to (59% vs. 41%), and age at diagnosis as 40 5.32), with no age difference be- 70 (Figure rea- tween the genders. The most common in SAH was diagnosis aneurysm for son 224 (84%). Of those with an unruptured aneurysm, 12 (4%) were symptomatic. had aneurysms. A total of 92 (34%) patients or PICA an- multiple aneurysms; several VA were diagnosed in 12 (4%) (Table eurysms 5.32), among whom 3 had also addition- com- elsewhere. The most aneurysm(s) al mon associated aneurysms were that of the with aneurysm(s) 5.33). Patients MCA (Table in the anterior circulation accounted for 75 125 150 100 - - - 51 - 5 (7) 2 (3) 14 (20) Left; No.(%) 5 (7) 2 (3) 11 (16) 31 (44) Aneurysms of the vertebral and Right; No.(%) posterior inferior cerebellar arteries VA Hypoplasia Atresia PICA Hypoplasia Extracranial origin rysm was diagnosed in 1961. After 1990 1990 After in 1961. diagnosed was rysm 78% of the patients were admitted, and af or PICA MRA in our department − a VA Overview of patients with vertebral artery or posterior inferior cerebellar artery aneurysms Patients and aneurysms VA 284 altogether had 268 patients The aneu VA first The aneurysms. PICA and ference in mean width or thickness between and the tubercles (on the right side 11.2 mm 6.3 and mm 10.9 left the on and mm, 6.1 association appeared between size mm). No of the tubercle and side of the aneurysm. all in- 5.31). Among ter 2000, 56% (Figure tracranial aneurysm patients admitted after and CTA of use routine of era the − 2000 The right jugular tubercle was slightly lon- The right jugular tubercle was slightly on ger (p = 0.04), with its mean diameter side 17.6 the right side 18.4, and on the left 5.24 demonstrates the location mm. Figure dif of the jugular tubercle. There existed no PICA, posterior inferior cerebellar artery; PICA, posterior inferior vertebral artery VA, Variation in the VA and PICA VA in the Variation Table 5.26 Table Vkirja_viite_255246_LEHTO_.indd 49 Table 5.31. Figure 5.32 Characteristics of the whole patient population Patients according to age groups (n = 268) 80

Gender No. (%) Male 111 (41) 60 Female 157 (59) Age at primary median (range) diagnosis 40 All 52 (16 – 85) Presentation No. (%) SAH from VA or PICA 194 (74) 20 aneurysm SAH from another 29 (11) aneurysm 0 Mass effect 9 (3) ad20 20- 30- 40 50 60 70 80- Ischemia 3 (1) Ruptured AVM/AVF 1 (0,3) Incidental 32 (12)

AVF, arteriovenous fistula; AVM, arteriovenous malformation; PICA, posterior inferior cerebellar artery; SAH, subarachnoid hemorrhage; VA, vertebral artery

5.34), among them definite de-novo aneurysms were located at the junction of the rysms numbering four. Time from the first VA and PICA. Fusiform aneurysms were aneurysm diagnosis to the second ranged distributed more evenly, the most common from 3 to 38 years, with a mean of 15 years. locations being the distal PICA and distal Four-vessel angiography was primarily do- VA (Figures 5.33 and 5.34). Aneurysms sized ne for 221 (83%) patients, and at some point less than 7 mm accounted for 196 (68%). 227 (85%). Giant aneurysms were rare, diagnosed in Among the 268 VA and PICA aneurysms, only six patients. most were saccular, but the percentage of fusiform aneurysms was rather high, 28% Treatment (Table 5.35). Both saccular and fusiform VA Of all the patients, 225 (84%) had at least and/or PICA aneurysms were diagnosed in one aneurysm treated, 209 (78%) at least three patients. Of the fusiform aneurysms, one VA or PICA aneurysm treated. In two two were traumatic. Most saccular aneu- patients, not all VA and PICA aneurysms were treated. The most common reason 52 for conservative treatment was poor condi-

Vkirja_viite_255246_LEHTO_.indd 50 30.3.2015 15.09 Results Table 5.32. Table 5.33. Patients with multiple VA or Associated aneurysms PICA aneurysms (n = 12) (patients n = 85, aneurysms n = 161)

No. of patients No. of No. of Multiple distal PICA aneurysms patients 7 aneurysms only (% of all (% of all associated patients) 2 aneurysms 5 aneurysms 3 - MCA 76 (40) 53 (20) 4 1 ACA 24 (13) 22 (9) 5 1 ICA 34 (18) 26 (10) 2 VA aneurysms 3 BA 19 (10) 15 (6) 1 VA and 1 distal PICA 2 VBJ 3 (2) 3 (1) aneurysm PCA 5 (3) 5 (2) PICA, posterior inferior cerebellar artery; VA, vertebral artery ACA, anterior cerebral artery; BA, basilar artery; ICA, internal carotid artery; MCA, middle cerebral artery; PCA, posterior cerebral artery; VBJ, vertebrobasilar junction

Figure 5.33 Figure 5.34 Locations of saccular aneurysms (n = 202) Locations of fusiform aneurysms (n = 81)

37 4 19 22 114 14 16 3 8 5 10 9

53 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 51 30.3.2015 15.09

1 - 1 1 1 - No. of certain denovo aneurysms 1 - - 2 3 2 2 4 2 Total no. of Total aneurysms 3 3 2

(fus) a PICA (sac) AcomA (sac) PcomA (sac) PICA (sac), proximal VA distal PICA (sac) MCA (sac), PICA (sac) PICA (sac) proximal VA (sac) later; Location (morphology) Aneurysms diagnosed VA

(fus) a AcomA (sac), MCA (sac) PICA (sac) PICA (sac) MCA (sac), (sac) PComA VA PComA PComA (sac) PComA AcomA (sac), ICA (sac) MCA (sac) Aneurysms diagnosed first; Location (morphology)

16 6 13 2 8 22 50 10 Interval between diagnosis (years)

SAH SAH SAH SAH Suspected aneurysm in MRI Screening, PCKD SAH SAH Screening Reason for angiography later on

SAH SAH SAH SAH SAH SAH SAH SAH SAH Reason for primary diagnosis M M F F M F F M F Gender 36 44 44 64 35 28 29 32 35 Age at primary diagnosis Exact location not available AComA, anterior communicating artery; F, female; fus, fusiform; ICA, internal carotid M, male; MCA, middle AComA, posterior communicating artery; cerebral artery; MRI, magnetic resonance imaging; PCKD, polycystic kidney disease; PComA, vertebral artery PICA, posterior inferior cerebellar artery; sac, saccular; SAH, subarachnoid hemorrhage; VA, Table 5.34. 5.34. Table Additional aneurysm(s) found later a 54

Vkirja_viite_255246_LEHTO_.indd 52 30.3.2015 15.09 Results 30.3.2015 15.09 284 3 (1) 8 (3) 7 (2) 6 (2) 14 (5) 14 (5) 1 (<1) 17 (6) 23 (8) 10 (4) 10 (4) 91 (32) 81 (29) 96 (34) 155 (55) 164 (58) 114 (40) 202 (71) Total; No. (%) Total; - 84 4 (5) 4 (5) 3 (4) 5 (6) 2 (2) 2 (2) 2 (2) 6 (7) 8 (10) 13 (15) 51 (61) 51 (61) 10 (12) 35 (42) 27 (32) 23 (27) 57 (68) Unruptured; No. (%) Unruptured; 55 - 200 9 (5) 6 (3) 6 (3) 6 (3) 7 (4) 4 (2) 15 (8) 12 (6) 1 (< 1) 1 (< 1) 54 (27) 83 (42) 68 (34) 79 (40) 145 (73) 103 (52) 104 (52) Ruptured; No. (%) Ruptured; No. Aneurysms of the vertebral and posterior inferior cerebellar arteries 24 mm 14 mm – – VA, exact location NA VA, Morphology Saccular Fusiform NA prePICA postPICA fusiform, including origin of PICA Exact location NA distal PICA distal VA No of aneurysms Location Proximal VA no PICA VA, PICA Maximal size < 7 mm > 24 mm NA 7 15 NA, not available; PICA, posterior inferior cerebellar artery; VA, vertebral artery artery; VA, NA, not available; PICA, posterior inferior cerebellar Characteristics of VA and PICA aneurysms of VA Characteristics Table 5.35. 5.35. Table Vkirja_viite_255246_LEHTO_.indd 53 tion after SAH (n = 24) (Table 5.36). Most of Table 5.36. those treated conservatively because of an Reasons for conservative treatment of anticipated technical difficulty in surgery a VA or PICA aneurysm (patients 59) were diagnosed in the early part of the series. No. Among actively treated VA and PICA an- Poor grade after SAH 25 eurysms, surgically treated accounted for 198, endovascularly 14, and those treated by Technical reason 8 both methods 7 (Figures 5.35 to 5.37). Among Old age / severe general disease 6 the 156 saccular aneurysms, 145 (93%) were The wrong aneurysm treated surgically, 5 (3%) by embolization, 3 interpreted as a ruptured one and 5 (3%) by combined means. Active treatment of fusiform aneurysms was more vari- Reason not specified 3 able, with those surgically treated number- Rebleeding and death after a 3 ing 53 (82%), endovascularly 9 (14%), and negative angiography by both means 2 (3%). Mere clipping was Small aneurysm 3 done to 30 (47%) fusiform aneurysms. En- Spontaneous thrombosis of dovascular treatment was more common in 2 fusiform than saccular aneurysms (four ver- the aneurysm and vessel sus nine patients). The reason for multimo- Refused surgery 2 dality treatment was failed embolization in Followed up 1 two aneurysms, bleeding of a residive aneurysm after clipping in another two, incom- AVM-related (flow-related) aneurysm 1 plete occlusion, aneurysm perforation and Aneurysm missed in angiography 1 failed embolization, and failed proximal oc- Unruptured aneurysm 1 clusion in one aneurysm each. AVM, arteriovenous malformation; Outcome SAH, subarachnoid hemorrhage Angiographic Postoperative angiography after treatment of a VA or PICA aneurysm was performed on 185 (84%) aneurysms in 182 patients. The angiographic method was catheter angiography in 106 aneurysms (57%), CTA in 74 (40%), and both in 5 (3%) aneurysms. Among these, total occlusion was achieved for saccular aneurysms in 106 (91%), among those clipped 97 (90%); and for fusiform in 33 (63%), among those clipped 22 (79%). The best surgical results occurred in saccular distal PICA aneurysms, with 94% of the aneurysms totally occluded. After surgery, six aneurysms re-ruptured, and additionally one previously unruptured giant aneurysm ruptured after proximal oc- 56

Vkirja_viite_255246_LEHTO_.indd 54 30.3.2015 15.09 Results 30.3.2015 15.09

end-to-end anastomosis 0/1 Clipping and Resection and PICA re-clipping 2/2 partialis 1/0 PICA–PICA bypass,

clipping and resection

Proximal wrapping 1/0 occlusion and OA–PICA bypass and trapping 0/1 Clipping and resection 0/1 Trapping and Trapping resection 2/0

partialis 0/1 0/2 bypass 131/32 OA–PICA OA–PICA bypass and occlusion 1/1 and proximal trapping and resection occlusion 3/9 Mere clipping Mere trapping Mere proximal 57

0/1 0/3 135/32 Clipping Trapping Trapping Proximal Revascu- Aneurysms of the vertebral and Coagulation Coagulation Wrapping 1/2 Wrapping larization 2/4 occlusion 4/9 Resection 2/2 Exploration 1/0 posterior inferior cerebellar arteries Surgical treatment of VA and PICA aneurysms (saccular/fusiform) and PICA of VA Surgical treatment Figure 5.35. Figure 5.35. 145/53 Surgical Vkirja_viite_255246_LEHTO_.indd 55 Figure 5.36 Endovascular treatment of VA and PICA aneurysms (saccular / fusiform)

Endovascular 5/9

Mere Embolization Stenting Embolization Proximal embolization and stenting 0/2 and proximal occlusion 0/6 4/0 0/1 occlusion 1/0

With coils 0/4

With balloon 0/2

Figure 5.37 Multimodality treatment of VA and PICA aneurysms (saccular / fusiform)

Combined 5/2

Embolization and Clipping and Vertebral occlusion Clipping and clipping 4/0 embolization x 2 (coils) and vertebrail embolization 0/1 1/0 ligation x2 58

Vkirja_viite_255246_LEHTO_.indd 56 30.3.2015 15.09 Results Table 5.37. Patients/aneurysms with aneurysm rupture after treatment

Treatment Morphology / Time from Aneurysm Primary pre/post earlier treatment to Final GOS location occlusion (year of first ruptured rupture treatment) clipping Fusiform / Distal PICA Total 14 days (2005) / 3 ruptured coiling clipping Saccular / VA–PICA Total 3 years (2005) / 5 ruptured coiling x 2 proximal Fusiform / Distal VA Failed 17 days occlusion 1 ruptured (1998) / - Fusiform / clipping VA–PICA Partial 9 days 1 ruptured (2008) / - Saccular / No wrapping VA–PICA 13 years 1 ruptured angiography (1966) / - wrapping Saccular / No VA–PICA 0 days (1966) / proxi- 1 ruptured angiography mal occlusion Giant, saccular No VA 2 days Crutchfield / - 1 / unruptured angiography Fusiform / Proximal VA Partial 6 days stenting / - 1 ruptured

GOS, Glasgow outcome scale, PICA, posterior inferior cerebellar artery, VA, vertebral artery

clusion (Table 5.37). One dissecting aneu- was severe SAH (Table 5.38). Later, eight rysm ruptured after stenting. Of the eight patients died for aneurysm-related reasons: patients suffering from aneurysm rupture three in a rupture of a initially undiagnosed after treatment, only two survived. aneurysm (two VA and one AComA aneurysm), one with IVH from shunt removal, Clinical one with rupture of a previously conserva- Among patients with a minimal theoreti- tively treated incidental aneurysm, one for cal follow-up of one year, within one year re-rupture after the patient refused surgery, 70 (26%) died. The most common cause one from re-bleeding after aneurysm wrapping, one after hemiparesis caused by mass 59 effect of a residive VA aneurysm, and one Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 57 30.3.2015 15.09 of pneumonia after early removal of trache- Table 5.38. ostomy. Causes of death within one year after Among those 168 who survived and whose aneurysm diagnosis in 70 patients VA and PICA aneurysms were actively treated, 155 (92%) returned to an independent or No. of patients previous stage of life; 12 (7%) remained de- Related to VA aneurysm pendent on help, three were unable to live at home. One foreign patient was transferred Severe SAH 35 to her home country in poor condition and Per / post-treatment 5 was lost to follow-up. As mentioned, later, bleeding eight of these patients died of aneurysm-re- Unruptured aneurysm lated causes. initially operated 3 on unintentionally 5.4 Patients with ruptured vertebral Brain infarction or posterior inferior cerebellar artery aneurysms Spasm 3 Patients and aneurysms Vessel occlusion 2 Of the 268 patients, those primarily present- Pneumonia 6 ing with a ruptured VA or PICA aneurysm accounted for 194, giving an incidence of Pulmonary embolism 1 5.3% among all ruptured aneurysms. Mul- Myocardial infarction / 3 tiple aneurysms were diagnosed on admis- insufficiency sion in 47 (24%) patients (Table 5.41); multi- Trauma 2 ple VA or PICA aneurysms were diagnosed in 8 (4%). Anterior circulation aneurysm(s) Unrelated to VA aneurysm occurred in 37 (19%) and an additional pos- Severe SAH 6 terior circulation aneurysm in 8 (4%) pa- Cancer 3 tients. Later, two patients were diagnosed Cardiac infarction 1 with one de -novo aneurysm each, one in the PComA and the other in the proximal SAH, subarachnoid hemorrhage; VA. VA, vertebral artery In addition, four patients later suffered a second SAH caused by a previously undiagnosed VA or PICA aneurysm (Table 5.42), and one conservatively treated incidental fusiform VA aneurysm ruptured 3.5 years after diagnosis. grades 3-5) 68 (35%). Among patients with Table 5.43 presents patient characteris- CT, Fisher grade 1 was true of 6 (4%), grade tics. Women numbered 112 (58%). Median 2 in 12 (7%), grade 3 in 24 (14%), and grade age at diagnosis was 51, with most admitted 4 in 128 (75%). Figure 5.42 shows a typical at age 40 to 49 (Figure 4.41). No difference hemorrhage caused by a ruptured PICA an- emerged in age between men and wom- eurysm. en (p = 0.27). Preoperatively good grade Among the 194 ruptured VA and PICA (Hunt&Hess grades 1-3) patients numbered aneurysms, those saccular accounted for 126 (65%) and poor grade (Hunt&Hess 140 and fusiform 53 (Table 5.44). Morphol- ogy of one ruptured aneurysm was unavail- 60 able. Figures 5.43 and 5.44 show locations

Vkirja_viite_255246_LEHTO_.indd 58 30.3.2015 15.09 Results Table 5.41. Figure 5.41 Associated aneurysms Age groups at diagnosis 50 No. of No. of patients aneurysms (% of all (% all 108 associ- 194 patients) 40 ated aneurysms) MCA 31 (48) 26 (13) 30 ICA 16 (25) 12 (6) ACA 7 (11) 6 (3) BA 5 (8) 4 (2) 20 PCA 4 (6) 4 (2) 10 Abbreviations as in Table 5.33

0 ad20 20- 30- 40 50 60 70 80-

Table 5.42. Patients with a VA/PICA aneurysm rupture after rupture of another aneurysm

Interval Age at The first between The second GOS GOS after primary ruptured diagnosis ruptured after the the second diagnosis Gender aneurysm (years) aneurysm first SAH SAH AComA 29 F 50 PICA (sac) 5 1 (sac) proximal VA 32 M MCA (sac) 10 5 1 (sac) AComA 36 M 16 PICA (sac) 5 3 (sac) 64 F MCA (sac) 2 PICA (sac)a 5 4

a Definite de-novo aneurysm AComA, anterior communicating artery; F, female; GOS, Glasgow outcome scale; M, male; MCA, middle cerebral artery; PICA, posterior inferior cerebellar artery; SAH, subarachnoid hemorrhage; VA, vertebral artery 61 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 59 30.3.2015 15.09 Table 5.43. Figure 5.42 a and b. Characteristics of those with a ruptured Typical hemorrhage pattern after rupture VA or PICA aneurysm of a PICA aneurysm

Age median (range) All 51 (16 – 82) Male 53 (16 – 82) Female 51 (17 – 79) Gender No. (%) Male 82 (42) Female 112 (58) Hunt&Hess grade 1 33 (17) 2 49 (25) 3 44 (23) 4 34 (18) 5 34 (18) No. of aneurysms 1 147 (76) 2 35 (18) 3 7 (4) 4 1 (1) 5 1 (1) 6 2 (1) 7 1 (1)

Vkirja_viite_255246_LEHTO_.indd 60 30.3.2015 15.09 Results of the aneurysms in saccular and fusiform Figure 5.42c groups, showing more men in the fusiform Typical hemorrhage pattern after aneurysm group (39% of all men versus rupture of a PICA aneurysm 19% of women, p = 0.003). No age difference appeared between patients with saccular and fusiform aneurysms (p = 0.80). Sac- cular aneurysms were located more often on the left side (67% versus 33%, p = 0.013) and were smaller than those fusiform (p = 0.01). Comparing patients with a ruptured VA or PICA aneurysm to those with another ruptured aneurysm, the patients were older, and their Fisher grade was higher, due to frequent IVH (Table 5.45). They also ex- perienced re-bleeding more often before treatment (p = 0.001); in further analysis, this was true for distal PICA aneurysms (p < 0.001), but not for VA aneurysms (p = 0.10). Among the patients with a ruptured distal PICA aneurysm, the first rebleeding occurred within 3 hours in 10 (42%), in 3 to 12 hours in 4 (17%), in 12 to 24 hours in 2 (8%), and after 24 hours in 9 (38%). Com- pared to other ruptured aneurysms, VA and PICA aneurysms were smaller and more often fusiform. them, 111 (94%) were treated surgically, and Treatment and angiographic outcome endovascularly 4 (3%) (Figures 5.45 and Of the 31 patients treated conservatively, 15 5.46). Treated with both methods were 3 were of H&H grade 5. Due to an anticipated (3%): one was clipped after partial emboli- technical difficulty in surgery six were treat- zation, the other after coil extravasation and ed conservatively: four in 1970s, and one in incomplete occlusion, and one was initial- both the 1980s and the 1990s. One fusiform ly clipped but re-ruptured and was subse- (traumatic) aneurysm and its parent vessel quently coiled twice. thrombosed spontaneously. The aneurysm In the 1960s, two aneurysms were was missed in angiography in one patient; in wrapped. One re-bled the same day, and was three others, angiography was negative. Ver- treated with proximal occlusion. The other tebral angiographies were not done initially re-ruptured 13 years later, and the patient in three patients, and an anterior circulation died. Additionally, in the early part of the aneurysm was incorrectly considered to be series, three aneurysms were treated with the ruptured. One patient refused treatment. proximal occlusion. Later, one patient was treated with partial VA occlusion and OA– Saccular aneurysms PICA bypass. One cortical partially throm- Actively treated ruptured saccular VA and bosed distal PICA aneurysm was resected. PICA aneurysms numbered 118. Among Postoperative angiography was performed for 97 (82%) patients; among those 63 with clipped aneurysms for 88 (85%). All Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 61 30.3.2015 15.09 Fig 5.43 Fig. 5.44 Locations of ruptured saccular aneurysms Locations of ruptured fusiform aneurysms

27 2 12 14 76 13 14

5 2 6 6

the patients with no postoperative angi- rysms re-ruptured after treatment: one after ography done were admitted before 1998. stenting, one after proximal occlusion, and The angiography method was DSA in 60 two after clipping (see Table 5.37). (62%), CTA in 36 (37%), and both in 1 (1%) aneurysms. Of all the aneurysms treated, to- Clinical outcome tal occlusion was achieved in 91 (78%), in Follow-up time clipped aneurysms in 76 (86%) of cases. Af- Mean follow-up time was 7.9 years (median ter 2000, among clipped aneurysms, total 4, range 0 – 42). Total follow-up time was 1 occlusion was achieved in 45 (94%). Three 535 patient years. aneurysms re-ruptured after treatment (see Table 5.37). Mortality Among the 60 (31%) who died within one Fusiform aneurysms year, most died from severe bleeding (Table Actively treated fusiform aneurysms num- 5.46). From postoperative re-bleeding died bered 45. Among them, those treated surgi- four (7% of deaths), and from difficulties in cally were 39 (87%), and endovascularly 5 correct diagnosis of a ruptured aneurysm (11%), and with both methods, one. One fu- seven (12%). siform (dissecting) distal PICA aneurysm Risk factors for death at one year after ac- re-ruptured after total clipping initially; the tive treatment of the ruptured aneurysm residive was coiled together with the PICA. were in univariate analysis male gender Postoperative angiography was per- (p < 0.001), old age (p < 0.001), and poor formed for 39 (87%): 28 (72%) convention- H&H grade (p < 0.001). Fisher grade did al angiography or DSA and 11 (28%) CTA. A not reach statistical significance (p = 0.50), total occlusion was verified in 24 (65%), and nor did aneurysm size (p = 0.21), morphol- among the clipped in 17 (73%). Four aneu- ogy (p = 0.09), rebleeding before treatment (p = 0.53), shunt-dependent hydrocephalus 64 (p = 0.49) or decade of aneurysm treatment

Vkirja_viite_255246_LEHTO_.indd 62 30.3.2015 15.09 Results Table 5.44. Characteristics of ruptured VA and PICA aneurysms in fusiform and saccular groups a

Saccular; No. (%) Fusiform; No. (%) Total; No. (%) Number of aneurysms 140 53 193 Location Proximal VA 2 (1) 6 (11) 8 (4) VA–PICA junction 93 (66) 6 (11) 99 (51) prePICA 5 (4) - 5 (3) postPICA 76 (54) - 76 (39) fusiform, including - 6 (11) 6 (3) origin of PICA exact location 12 (9) - 12 (6) not available Distal PICA 40 (29) 28 (53) 68 (35) proximal 13 (9) 14 (26) 27 (14) distal 27 (19) 14 (26) 41 (21) Distal VA 2 (1) 12 (23) 14 (7) VA, no PICA - 1 (2) 1 (1) NA 3 (2) - 4 (2) Side Right 46 (33) 29 (54) 74 (38) Left 94 (67) 25 (47) 119 (62) Maximal size < 7 mm 77 (55) 22 (42) 99 (51) 7 – 14 mm 56 (40) 25 (47) 81 (42) 15 – 24 mm 2 (1) 5 (9) 7 (4) > 24 mm - - - NA 5 (4) 1 (2) 6 (3)

a Morphology of one aneurysm not available NA, not available; PICA, posterior inferior cerebellar artery; VA, vertebral artery

65 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 63 30.3.2015 15.09 0.58 0.23 0.01 p value < 0.001 < 0.001 Other 1287 (30) 4214 (97) 93 (2) 22 (1) 1363 (31) 1967 (45) 384 (9) 60 (1) 555 (13) 2410 (56) 3042 (70) 52 (12 – 92) No. (%) 1919 (44) 4329 median (range) 49 (1 – 92) 47 (1 – 88) VA or PICA VA 44 (26) 118 (71) 49 (29) - 84 (50) 70 (42) 7 (4) - 6 (4) 97 (58) 123 (74) 51 (27 – 79) No. (%) 70 (42) 167 median (range) 52 (27 – 79) 53 (29 – 78) Aneurysm morphology Saccular Fusiform Maximal size < 7 mm 7 – 14 mm 15 – 24 mm NA Multiple NA > 24 mm Number of aneurysms Single Female Gender Male Female Age at diagnosis (years) All Male Number of aneurysms Table 5.45. 5.45. Table or PICA aneurysm compared to patients with other ruptured aneurysms Patients with a ruptured VA

Vkirja_viite_255246_LEHTO_.indd 64 30.3.2015 15.09 Results a 0.23 0.001 < 0.001 < 0.001 < 0.001 237 (6) 394 (9) 1256 (29) 1687 (39) 755 (13) 2483 (57) 1039 (24) 807 (19) 2354 (54) 1221 (28) 754 (17) 809 (19) 1211 (28) 867 (20) 757 (18) 565 (13) 120 (3) 3318 (77) 922 (21) 89 (2) 6 (4) 11 (7) 24 (14) 119 (71) - 46 (28) 117 (70) 2 (1) 153 (92) 5 (3) 9 (5) 23 (14) 44 (26) 40 (24) 29 (17) 31 (19) - 110 (66) 55 (33) 2 (1) Fisher grade 1 1 3 NA IVH No Yes ICH No Yes Hunt&Hess grade 1 2 3 4 NA Rebleeding before treatment No Yes NA 4 NA NA 5 No difference between groups in time from rupture to occlusion of aneurysm (p = 0.52) ICH, intracerebral hemorrhage; IVH, intraventricular NA, not available; a

67 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 65 30.3.2015 15.09 1 clipping 2 coiling x 2 Coiling and Coiling treatment 3 Clipping and Multimodality 4 Embolization 1 118 Total Exploration

1 Exploration

1 2 Mere proximal wrapping Wrapping Wrapping occlusion 1 Wrapping and Wrapping

5 3 occlusion partialis VA 1 occlusion partialis VA OA-PICA bypass and proximal proximal Proximal occlusion occlusion occlusion 1 Wrapping and Wrapping Mere proximal

1 101 103 Mere clipping Clipping resection 1 re-clipping Clipping and Clipping and • Including one string ligation string one Including • twice entered occl. wrapping+prox with patient • Figure 5.45. Figure 5.45. of ruptured saccular aneurysms Treatment 68

Vkirja_viite_255246_LEHTO_.indd 66 30.3.2015 15.09 Results 2 Stenting 1 Clipping and coiling 2 Resection 2 2 49 Total Mere wrapping Wrapping 2 Trapping

1 2 9 (coils) (clip) 6 Proximal Proximal (balloon) occlusion occlusion VA occlusion VA occlusion VA

25 27 Mere clipping Clipping resection 2 Clipping and Figure 5.46 Figure 5.46 of ruptured fusiform aneurysms Treatment 69 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 67 30.3.2015 15.09 Table 5.46. Table 5.47. Causes of death within one year after diagno- Complications among actively treated patients sis of a ruptured VA or PICA aneurysm (n = 60) No. (%) No. of patients Brain infarction 43a (29) Severe SAH 35 Aneurysm rebleeding 4 (2) Per / post-treatment Postoperative 4 7 (4) bleeding hematoma Unruptured aneurysm Shunt dependent 38 (23) treated first 3 hydrocephalus unintentionally Infection Brain infarction Meningitis 19 (12) Spasm 3 Wound infection 6 (4) Vessel occlusion 1 Sepsis 14 (9) Pneumonia 6 Suspected 76 (47) Cardiac infarction / pneumonia 4 insufficiency Urinary tract 46 (28) Trauma 2 infection Pulmonary embolism 1 Peritonitis 2 (1) Cancer 1 Cardiac infarction 4 (2) Pulmonary embolism 2 (1) SAH, subarachnoid hemorrhage Deep venous 2 (1) thrombosis Gastrointestinal 3 (2) bleeding a No CT, MRI or autopsy in 15 patients

(p = 0.24). In multivariate analysis, inde- 43 (26%); 15 (9%) had no a post-operative pendent risk factors were male gender (OR scan or autopsy. One patient required sub- 1.917, CI 2.417–9.148), old age (OR 0.065, CI occipital craniectomy due to a cerebellar in- 0.898–0.977), high H&H grade (OR 1.452, farction; that patient returned to part-time CI 1.567–11.637), and larger aneurysm size work. One cerebellar infarction was resect- (OR 2.413, CI 1.126–110.710). ed but the patient did not recover. One patient underwent both infarction resection Complications and decompressive craniectomy; he re- Complications among patients with a treat- turned to independent life. Ventriculostomy ed ruptured aneurysm are in Table 5.47. Af- was done for 51 (26%) patients; those who ter treatment of the aneurysm, at least an- developed shunt-dependent hydrocephalus giographic vasospasm was diagnosed in 44 numbered 38 (20%). (27%) patients. Infarction was diagnosed in Four patients suffered from re-bleeding of a treated aneurysm. One operation was in- 70 terruptured due to aneurysm rupture when

Vkirja_viite_255246_LEHTO_.indd 68 30.3.2015 15.09 Results Table 5.48. Cranial nerve deficits

Pre- Post- operative, operative; Total Partial No No. (%) No. (%) recovery recovery recovery Dead Laryngeal palsy 2 (1) 52 (32) 22 20 2 8 Diplopia 8 (5) 24 (16) 16 2 2 4 Facial nerve deficit - 5 (3) 1 - 2 2 Trigeminal deficit - 2 (1) - - 2 - Hearing loss - 1 (1) 1 - - - Accessory nerve - 5 (3) 3 - 2 - deficit NA 53 (33) 14 (9)

NA, not available

opening the dura. A postoperative hemato- Cranial nerve deficits ma was diagnosed in seven patients, four of Among the 155 patients operated for a rup- these caused by ventriculostomy or shunt tured aneurysm, on admission a cranial nerve insertion. Three of the hematomas required deficit was present in 10 (6%) patients who evacuation. could be examined; due to their poor condi- Culture-positive meningitis was diag- tion, 53 (33%) patients could not be examined nosed in 19, and among them, 2 also had a properly (Table 5.48). After surgery on the an- wound infection. Mere wound infection was eurysm, 50 (32%) had a deficit; those not ex- diagnosed in four patients. No lambeau re- amined accounted for 14 (9%). Postoperative- moval was needed due to infection. Septi- ly, laryngeal palsy was most common, in 36% cemia was diagnosed in 15; 8 of them also of patients examined. Tracheostomy was nec- having meningitis. Pneumonia was at least essary for 33 (23%). Most patients recovered; suspected in 76 patients, and urinary tract two were left with a tracheostomy and PEG, infection in 46. Those diagnosed with any and one died of pneumonia after early re- infection numbered 106 (65 %). moval of the tracheostomy in a hospital else- Additionally, the two patients with pul- where. Among those endovascularly treated, monary embolism also had a deep venous only one patient suffered from a cranial nerve thrombosis. Of the three patients with gas- deficit: it caused him diplopia. trointestinal bleeding, one had bowel perforation. Additionally, one patient suffered Overall outcome from peritonitis, but with no perforation ev- Within one year, 60 patients died. Among ident. those who survived for more than one year of follow-up, those recovering to their former or an independent state of life num- 71 bered 123 (92%); 10 (9%) patients remained Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 69 30.3.2015 15.09 Table 5.51. Fig 5.51. The 69 patients with only unruptured Age distribution of the same 69 patients VA and or PICA aneurysms 50

Gender No. (%) Male 27 (39) 40 Female 43 (61) Age at primary diag- median (range) 30 nosis All 56 (16 – 85) 20 Decade of treatment No. (%) 1960s 3 (4) 1970s 2 (3) 10 1980s 3 (4) 1990s 8 (12) 0 ad20 20- 30- 40- 50- 60- 70- 80- 2000 - 54 (77) Presentation No. (%) SAH from another 25 (42) aneurysm Mass effect 9 (13) Ischemia 3 (4) Ruptured AVM/AVF 1 (1) Incidental 32 (46)

Abbreviation as in Table 5.31

dependent on help: one poor-grade patient PICA aneurysm(s), or both. Most were in- died 13 months after bleeding, six returned cidental findings (n = 32), or diagnosed in home, three were unable to live at home. Ad- addition to a ruptured aneurysm elsewhere ditionally, one poor-grade patient was trans- (n = 25) (Table 5.51). Table 5.51 shows pa- ferred to his home country in poor condition tient characteristics; additionally, age distri- and was lost to follow-up. bution is shown in Figure 5.51. After 2000, the number treated amounted to 77% of the Patients with unruptured patients. vertebral artery or posterior inferior cerebellar artery aneurysms Ruptured aneurysm in another location Overview Patients and aneurysms Among the total of 268 patients, 70 (26%) We had 25 patients initially diagnosed with were diagnosed with only unruptured VA or a ruptured aneurysm outside the VA and PICA; additionally, 4 patients were primari- 72 ly diagnosed with a ruptured aneurysm else-

Vkirja_viite_255246_LEHTO_.indd 70 30.3.2015 15.09 Results 30.3.2015 15.09

- No. 8 5 4 4 2 19 7 4 2 - 19 10 The location of the ruptured aneurysm was Patient characteristics are shown in Table characteristics are shown in Table Patient Location of the ruptured aneurysm MCA BA ICA ACA VBJ Locations of other aneurysms MCA ICA BA ACA VBJ VA distal PICA ACA, anterior cerebral artery; BA, basilar artery; ACA, anterior cerebral artery; BA, basilar artery; ICA, internal carotid artery; MCA, middle cerebral artery; PICA, posterior inferior cerebellar artery; vertebral artery; VBJ, vertebrobasilar junction VA, Table 5.53. 5.53. Table all the aneurysms Locations of cular. One patient had five small saccular dis- cular. tal PICA aneurysms together with a posterior where, and later with SAH from a primarily where, and later with SAH from a primarily or PICA undiagnosed aneurysm in the VA 5.34). (see Table 5.52. There was female predominance (19 dis age in difference no but 6), versus genders emerged between the tribution grade (H&H grades 1–3) (p = 0.45). Good accounted for 17 (67%). the MCA in 8 (32%) patients, and in the posterior circulation in 7 (28%) patients (Table 5.53). All the ruptured aneurysms were sac- 73 median (range) 52 (27 – 71) 56 (44 – 63) 51 (27 – 71) No. (%) 6 (25) 19 (75) 1 (4) 1 (4) 2 (8) 3 (13) 18 (71) 4 (4) 7 (25) 6 (25) 2 (8) 6 (25) - 8 (33) 8 (33) 4 (17) 2 (8) 2 (4) 1 (4) Aneurysms of the vertebral and posterior inferior cerebellar arteries Age All Male Female Gender Male Female Decade of admission 1960s 1970s 1980s 1990s 2000 - Hunt&Hess grade 1 2 3 4 5 No. of aneurysms 1 2 3 4 5 6 7 Patient characteristics of those 25 with a ruptured of those 25 with Patient characteristics and PICA the VA aneurysm outside Table 5.52. 5.52. Table Vkirja_viite_255246_LEHTO_.indd 71 Table 5.54. Table 5.55. VA and PICA aneurysms associated Patients with AVMs with ruptured aneurysms elsewhere Total no. No. Cause of of aneu- Locations of the VA / Age Gender bleeding rysms PICA aneurysm 44 F AVM 2 proximal VA 1 Aneurysm 69 F 3 PICA (prePICA) prePICA 1 Aneurysm postPICA 15 62 M (distal 3 PICA) distal PICA 10 Aneurysm exact location NA 2 57 F 6 (BA) distal VA - Aneurysm Morphology 63 F (distal 1 Saccular 25 PICA) Fusiform 3 AVM, arteriovenous malformation; Maximal size BA, basilar artery; M, male; F, female; PICA, < 7 27 posterior inferior cerebellar artery 7 – 14 2 15 – 24 - > 24 -

Abbreviations as in Table 5.44

fossa AVM. Otherwise no multiple VA and/ treatment of the VA or PICA aneurysm was or distal PICA aneurysms were found. Two poor condition after SAH in nine patients. distal PICA aneurysms and the proximal VA An additional 11 aneurysms were clipped, aneurysm were fusiform (Table 5.54). No an- after which one residual aneurysm was em- eurysm was diagnosed over 15 mm of a size. bolized twice.

Treatment Outcome The ruptured aneurysm was treated in 22 Of the 12 patients with actively treated VA patients, and VA or PICA aneurysm(s) was or PICA aneurysm, all recovered to the pre- treated in 12. In one patient with an AVM vious or an independent state of life. Six re- and multiple small distal PICA aneurysms, turned to work. the two largest aneurysms were clipped; oth- Postoperatively, three patients had a ers disappeared after removal of the AVM. hoarse voice without swallowing difficulties. The most common reason for conservative All recovered fully. One patient with a distal PICA aneurysm had a postoperative acces- 74 sory palsy that did not resolve.

Vkirja_viite_255246_LEHTO_.indd 72 30.3.2015 15.09 Results

30.3.2015 15.09 artery; VA, vertebral artery vertebral VA, artery; cerebellar inferior posterior PICA, artery; occipital OA, available; not NA, male; M, score; outcome Glasgow GOS, female; F,

resection

2011 Total 4 and clipping Hemiparesis 28 saccular postPICA F 57

PICA–PICA bypass, bypass, PICA–PICA

resection

2010 Total 5 and trapping Balance disturbance Balance 44 fusiform PICA distal M 58

OA–PICA bypass, bypass, OA–PICA

pimg later hemiparesis, oculomotor paresis oculomotor hemiparesis, later

2006 Total 1 20 saccular postPICA F 81

- re-clip and Clipping spasm: hemifacial Primarily

graphy resection

2008 5 Tetraparesis 36 fusiform VA distal M 51

No angio- No Trapping and partial partial and Trapping

2004 Total 3 Resection Dysmetria 60 saccular PICA distal F 73

2001 Total 5 Resection spasm Hemifacial 34 saccular NA M 42

hearing loss hearing

1994 - NA Conservative 20 fusiform VA distal F 55

paresis, abducens and Trigeminal

graphy resection paresis, dysphagia, dysartria, dizziness dysartria, dysphagia, paresis,

1984 5 postPICA saccular postPICA M 54 50

No angio- No and Clipping Oculomotor-, facial-, and accessory-nerve accessory-nerve and facial-, Oculomotor-,

graphy

1965 NA saccular NA F 16 Ataxia, dysphagia, dysartria, nystagmus dysartria, dysphagia, Ataxia, 50 Proximal occlusion Proximal 1 No angio- No

Aneurysms of the vertebral and

treatment morphology Gender Age Symptom (mm) Treatment Occlusion GOS

posterior inferior cerebellar arteries

Location; Size Size Year of of Year

aneurysm the by caused effect mass with those of Characteristics Table 5.56 5.56 Table Vkirja_viite_255246_LEHTO_.indd 73 Fig 5.52. Table 5.57. MRI of a patient with partially Characteristics of patients with incidental thrombosed giant VA aneurysm or screened aneurysms (n = 32)

Diagnosis No. (%) Incidental 28 (88) Screening 4 (13) Age median (range) All 58 (34 – 85) Male 60 (34 – 85) Female 56 (37 – 65) Gender No. (%) Male 15 (47) Female 17 (53) Decade of admission No. (%) 1970s 1 (3) 1970s 1 (3) 1980s - Ruptured arteriovenous malformation 1990s 2 (6) Among the five patients with AVM in the series, one presented with rupture of an AVM 2000 – 28 (88) (Table 5.55). Along with extirpation of the No. of aneurysms No. (%) ruptured AVM, the postPICA aneurysm was 1 21 (66) clipped, and the aneurysm in the tonsillo- 2 3 (9) medullary segment of PICA was treated by proximal occlusion. Neither aneurysm was 3 5 (16) visible in the postoperative DSA. Postoper- 4 - atively, the patient had a laryngeal palsy and 5 2 (6) diplopia; both symptoms resolved, and the 6 - patient returned to work. 7 1 (3) Mass effect Patient and aneurysm characteristics Nine patients were diagnosed because of each aneurysm was partially thrombosed. cranial nerve and brainstem compression Figure 5.52 demonstrates a giant aneurysm caused by the aneurysm (Table 5.56). Patient with brainstem compression. age ranged from 16 to 81. Those originating from the VA accounted for seven (with ex- Treatment act location of the origin in the VA unknown The various treatment methods are in Ta- in two), and those from the distal PICA two. ble 5.56. One aneurysm was re-clipped; the Fusiform aneurysms accounted for three; patient suffered primarily from hemifacial spasm, and the aneurysm was clipped with 76 a small neck remnant. Later, at the age of

Vkirja_viite_255246_LEHTO_.indd 74 30.3.2015 15.09 Results Table 5.58. Table 5.59. Associated aneurysms in patients with VA and PICA aneurysms associated incidental VA aneurysms with ruptured aneurysm elsewhere

No. of No. of No. aneurysms patients Locations of the ICA 1 1 VA / PICA aneurysm MCA 14 8 proximal VA 2 ACA 5 5 PICA PCA 1 1 prePICA - BA 5 3 postPICA 17 VBJ 1 1 including origin of 3 PICA Abbreviation as in table 5.53 distal PICA 2 distal VA 5 VA, no PICA 2 exact location 1 in VA NA Morphology Saccular 21 85, she developed a hemiparesis caused by Fusiform 11 a 27-mm residive aneurysm. Another com- Maximal size plex VA aneurysm was treated conservative- < 7 mm 15 ly because of assumed technical difficulties in the beginning of the 1990s. 7–14 mm 8 15–24 mm 6 Outcome > 24 mm - Two patients died: the 85-year-old with a hemiparesis from the residive aneurysm Abbreviations as in Table 5.44 did not survive, and a young patient suffered from aneurysm rupture a few days after VA occlusion in 1965. The only patient who received conservative treatment is still alive. Among the rest, four patients returned to work, one to independent life, and one re- Ischemia mained dependent on external help. Patient and aneurysm characteristics Among those treated actively, all but one Three patients presented with ischemia: had a laryngeal palsy postoperatively, three two men and one woman, aged 40 to 60. requiring a tracheostomy. Two died, one had Two aneurysms were located in distal VA a permanently hoarse voice, the remaining and one in distal PICA. All were fusiform. five made a full recovery. One aneurysm and the VA were thrombosed at diagnosis and another partially 77 thrombosed. Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 75 30.3.2015 15.09 Treatment was performed on three suspected familial The patient with the totally thrombosed aneurysm carriers, and on one of whom also VA and aneurysm was treated conserva- having PCKD. tively. The partially thrombosed aneurysm The characteristics of these 32 patients was treated with VA balloon occlusion, after are presented in Table 5.57. No statistical which the VA and the aneurysm throm- significance emerged for age by genders bosed totally. The proximal distal PICA an- (p = 0.19). Nearly all (80%) patients were eurysm was trapped after OA–PICA bypass. diagnosed after 2000. Multiple aneurysms were diagnosed in 11 (32%) patients (Table Outcome 5.58). Associated aneurysm(s) were found All the patients returned to work. The pa- in the anterior circulation in all the 11 patient treated with VA balloon occlusion al- tients. An additional posterior circulation ready had a laryngeal palsy before the treat- aneurysm outside VA and PICA was diag- ment; the palsy resolved partially during fol- nosed in four patients. No patient had mul- low-up, as also did his facial nerve deficit. tiple VA or PICA aneurysms or both a VA and PICA aneurysm. Incidental aneurysms Most aneurysms were located at the junc- Patient and aneurysm characteristics tion of the VA and PICA, postPICA aneu- In 28 patients the aneurysm was a mere rysms accounting for 17 (53%). Half of the incidental finding. Another four patients aneurysms were less than 7 mm in size, and were diagnosed because of screening, which a third were fusiform. (Table 5.59)

Table 5.60. Treatment of incidental VA and PICA aneurysms

Saccular Fusiform Total Clipping 9 3 12 Conservative 9 2a 11 Proximal occlusion Clip - 2 2 Coil - 2 2 Coiling (attempted), clipping x 2 1 1 Stenting and coiling - 1 1 Embolization and proximal occlusion with coils - 1 1 OA–PICA bypass and partial occlusion of VA with a clip - 1 1 Resection and PICA end-to-end anastomosis - 1 1

a Later, one aneurysm was clipped after its rupture OA, occipital artery; PICA, posterior inferior cerebellar artery; VA, vertebral artery 78

Vkirja_viite_255246_LEHTO_.indd 76 30.3.2015 15.09 Results Treatment and angiographic results and poor hearing; the facial paresis resolved Patients with an actively treated VA or PICA but the hearing did not improve. aneurysm numbered 22 (69%). Among the Fifteen patients returned to work and ten conservatively treated aneurysms, one is one to the previously independent life. A still followed up. Due to their old age, con- 65-year-old patient received help in house- servative treatment was the choice for three, keeping after the surgery. The patient with and due to a small aneurysm for one; one thrombosed PICA anastomosis died. patient was treated conservatively in the One conservatively treated incidental fusi- 1970s because of anticipated technical prob- form distal VA aneurysm ruptured three lems, and in the 1960s, unruptured aneu- years after the diagnosis. The aneurysm was rysms were not treated. clipped, but the patient did not survive. ❦ Table 5.60 shows treatment methods for the aneurysms. All the nine saccular aneurysms were clipped; eight were totally occluded; one had no postoperative angiography Treatment of fusiform aneurysms was more diverse. Three patients were treated by endovascular means. The aneurysm treated by stenting and coiling resulted in near-total occlusion, and the one treated with internal coiling was totally occluded. An endovascular occlusion of the VA by a large fusiform aneurysm failed, and the VA was closed surgically; finally this aneurysm thrombosed. Among patients treated with proximal occlusion, this was the only aneurysm proven to be thrombosed. One distal, large, partially thrombosed PICA aneurysm was resected, and the ends of the PICA sutured together. Another patient with a fusiform distal VA aneurysm was treated with an OA–PICA bypass, and the VA was occluded with a clip that was partially left open with the aid of absorbable string.

Outcome Postoperatively, nine patients suffered from cranial nerve deficits. Six had a laryngeal palsy; among these, one needed a tracheostomy. One died, another was left with a hoarse voice and slight swallowing difficulties; all the others made a full recovery. Two patients had accessory nerve paresis: one recovered totally, and the other partially. One patient had, postoperatively, facial paresis 79 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 77 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 78 30.3.2015 15.09 This retrospective series comprises 268 patients with 288 aneurysms in the VA and distal PICA. The patients were treated in Helsinki University Central Hospital, Finland, from 1961 to 2011. The present series describes characteristic features of the aneurysms, treatment, and outcome. This series is the largest reported up until now.

Incidence Few reports have been involved VA and distal PICA aneurysms without significant selection bias. Yamaura et al. in 1988 reported VA aneurysms to comprise around a third Discussion of all posterior circulation aneurysms (250). Among all saccular aneurysms, Huttunen et al. reported those located in the VA and distal PICA to comprise 2.4% (82). In our series after the year 2000, among all aneurysm patients, 5.1% had a VA or distal PI- CA aneurysm; among ruptured aneurysms, those of the VA or distal PICA comprised 3.9%. Compared to earlier figures, ours are somewhat larger. The difference may be ex- plained by a four-vessel angiography, MRA, or CTA for all our aneurysm patients, and in addition our material is non-selected, including also conservatively treated poor-grade patients. The short- coming of our figures is the absence of data on those who died before reaching the neurosurgical unit.

Anatomic features Location As in the earlier reports on VA aneurysms (11, 47, 250), also in our series the most frequent aneurysm location was the VA–PICA junction. Aneurysms in the distal VA are more common than in the proximal VA: in the series of Drake et al., proximal VA aneurysms numbered only 4, and distal 41 (47). In our series the difference was not that distinct: in the proximal VA 14 aneurysms and in the distal 81 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 79 30.3.2015 15.09 VA 23 aneurysms. Among distal PICA an- sia is also more common for the right VA, as eurysms, in all reports except one the major- it is also for the right PICA (93, 104), The rea- ity of aneurysms were located in medullary son for this asymmetry is not known. segments (78, 131, 167, 190, 227). This was con- Due to variations in anatomy of the VA and firmed also by our series, with 74% located PICA, the location of a PICA aneurysm in there, 17% in the telovelotonsillar segment, the posterior fossa is highly variable. Sever- and 9% in the cortical segment. al reports show a PICA aneurysm located extracranially or on the side of the skull contra- Morphology lateral to the origin of the parent artery (47, Many other series categorize the VA and 221, 248); in our series, one aneurysm was distal PICA aneurysms as saccular, fusi- located extracranially and four aneurysms form, and dissecting (11, 19, 47, 250). The were on the side contralateral to the parent number of non-saccular aneurysms in the artery. Distances of the aneurysm from the VA is high, ranging from 13 to 48% (11, 47, foramen magnum and midline are impor- 250), a wide range perhaps related to differ- tant for planning the site of the craniotomy ing definitions for non-saccular aneurysms and the extent of drilling the skull base (18, among series. Due to controversies over def- 115). Within our series, the distance of the initions, and lack of MRI in SAH patients aneurysm neck from the foramen magnum leading to difficulties in diagnosing classi- ranged from 1 mm below it to 31 mm above, cal signs of dissection, we limited our cat- and from the midline, 8 mm contralateral to egorization into saccular and fusiform. We 14 mm ipsilateral. Even if the size of jugu- classified as fusiform those aneurysms with lar tubercles ranges within a few millimeters, a neck larger than the aneurysm’s width; in noticing it is important in the tight space of our series the proportion of fusiform an- the posterior fossa. For example, too much eurysm in the VA was 22% and in the dis- of lateral tilting of the head can cause an an- tal PICA 43%. Additionally, among saccu- eurysm to be hidden behind a large tubercle. lar distal PICA aneurysms, classical saccu- Additionally, patients with distal PICA an- lar aneurysms at the branching point of an eurysms have a high incidence of different artery accounted for only 10%. vascular variations, anomalies and lesions (167, 174, 227), as confirmed also by our se- Anatomy of VA–PICA aneurysms in CTA ries, where only 19% patients had no vascu- Even if DSA is still the gold standard for an- lar deviation. The most common findings eurysm imaging, compared to DSA, CTA is were multiple aneurysms (26%), hypoplas- fast, cheap, non-invasive, more readily avail- tic VA (42%), and hypoplastic PICA (22%). able, and superior in visualization of the skull base and calcifications(233) . The liter- Treatment ature provides, however, only one study on Challenges related to treatment of VA and PICA aneurysms shown in CTA (248). distal PICA aneurysms result from ana- Anatomy of the VA and PICA is highly tomical relationships of the aneurysm to variable, with elongation on VA, tortuous the vasculature, the posterior cranial fos- course of both arteries, and variable location sa, brainstem, and cranial nerves, as well the PICA origin (136). As in earlier series (93, as its morphology and etiology. Despite re- 104), in ours the left VA was larger than the markable advances since the first success- right, with median diameter on the left side ful direct occlusion of an aneurysm in the 2.8 mm and on the right 2.1 mm. Hypopla- posterior circulation in 1946, treatment of dissecting VA aneurysms in particular still 82 needs improvement.

Vkirja_viite_255246_LEHTO_.indd 80 30.3.2015 15.09 Discussion

Surgical treatment and radiological outcome most common being PICA–PICA and The complexity and variance of the lesions, OA–PICA (9, 34, 123, 129, 161, 212). as well as passionate search for the best so- In the series of Drake et al., 86% of the lution, is reflected in the great variety of aneurysms became totally occluded, and 4% treatment methods and approaches. Tech- had a neck remnant (47). In a more recent niques more recently reported include clip- series, total occlusion was achieved in 93% ping (167, 227), trapping (35, 87, 204), wrap- of aneurysms; in this surgical series, dis- ping (204), proximal occlusion (35, 87, 204) secting VA aneurysms were referred to en- with or without different bypass procedures. dovascular surgery (204). In our series, total In contrast to endovascular surgery, micro- occlusion was achieved in 90% of clipped surgical occlusion of VA and distal PICA saccular and in 79% of clipped fusiform aneurysms meets challenges, especially the aneurysms, results consistent with those of necessity of avoiding cranial nerve deficits. other series. Regarding of the vasculature, for classical Postoperative angiography after treat- aneurysms at the VA–PICA junction, the ment of VA or PICA aneurysm was per- PICA is seldom compromised. Converse- formed on 181 patients: of the investigations, ly, for dissecting VA aneurysms, total and 57% were by DSA/conventional angiogra- stable occlusion with preservation of flow phy and 40% by CTA, with 3% imaged by is demanding. In proximal occlusion of fu- both methods. Total occlusion was achieved siform and dissecting VA aneurysms, good in saccular aneurysms in 106 (91%) (among outcomes are reported (47). Subsequent rup- those clipped 97 (90%)), and in fusiform tures, however, are detectable, both by oth- ones in 34 (63%) (among those clipped 22 ers (102, 109) and in our series. One cause of (79%)). The best results were in saccular differing success may lie in the timing of distal PICA aneurysms with all but one to- treatment: re-rupture rate is highest with- tally occluded. Even DSA was performed if in the first day after the first ictus, and de- in doubt about a neck remnant after CTA, creases thereafter (147, 247). To our knowl- some neck remnants may have been missed edge, no randomized trial covers the best in cases without titanium clips used. treatment of dissecting VA. Based on the literature and our experience, at least consider Endovascular treatment and trapping the whole diseased segment, with radiological outcome a bypass if needed. Although the present series has a strong Beside fusiform aneurysms, another surgical focus, within the last ten years challenge are giant aneurysms. Many most published series are purely endovas- times these patients are already inva- cular (for the recent published series, see lidized by brainstem and cranial nerve Table 2.33). Unfortunately, the emphasis on deficits (47). Compared to endovascular surgery in the present series makes com- surgery, microsurgery, if needed, has the parison between surgical and endovascular advantage of debulking the mass of the treatment impossible. aneurysm. Yet the challenge is operating Endovascular treatment escapes the risk in the posterior fossa made even tighter of causing cranial nerve deficits. It is, how- by the aneurysm. Another advantage of ever, challenged by preserving the flow in surgical treatment is the possibility of do- the PICA, as the PICA often courses inferi- ing a bypass if blood flow is compromised. orly at a sharp angle when leaving the VA. Several different bypass options exist, the In distal PICA aneurysms, aneurysms with well-defined necks can be embolized, but 83 fusiform distal PICA aneurysms present a Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 81 30.3.2015 15.09 challenge. In aneurysms distal to the choroi- need to be combined with bypass. The ef- dal point, occlusion of the artery can be con- fectiveness of flow-diverters in these aneu- sidered (92). Using stents in a small-caliber rysms is still to be shown. In giant aneu- artery is for the moment not recommended rysms, direct clipping together with resec- (5). Reducing the mass effect is uncertain in tion or bypass if needed is an option, with the use of endovascular techniques in com- a significant risk for laryngeal palsy. Mere plex aneurysms (86). coiling carries the risk of coil impaction, As treatment of ruptured dissecting VA which may lead to problems in mass ef- aneurysms have been challenging by both fect. In some cases, embolization or proxi- endovascular and exovascular means, in the mal occlusion may be combined with a by- future, flow-diverters may become a treat- pass operation. ment of choice. For the moment, however, series on their use in these lesions are Outcome scarce (25, 182); especially series on ultra-ear- The overall outcome of treating VA and dis- ly treatment of the dissecting aneurysms tal PICA aneurysms is favorable, with 80 would be essential. to 85% recovering at least to an indepen- Angiographic results in a recent study dent stage of life (67, 78, 131, 167). In our se- on endovascular PICA aneurysms showed ries, mortality within one year of the diag- complete occlusion in 63% (24). In a series nosis was high, with nearly a third deceased, on internal trapping of ruptured dissecting mainly due to their severe initial bleeding. VA aneurysms, 21% of those initially totally Those who survived, however, made a good occluded re-canalized, reminding us of the recovery, with only 7% not regaining inde- need for follow-up. pendence. Additionally, we found a rather high Choosing treatment modality and techniques rate, 9%, of recurrent SAH occurring lat- Even if treating cerebral aneurysms treat- er. Wermer et al. in 2005 calculated the in- ment is always planned in a case-by-case cidence of new bleeding to be 3% within ten manner, this need is even more pro- years (242). Our high number can in part re- nounced in aneurysms of the VA and PI- sult from suboptimal aneurysm occlusion, CA. For VA and proximal PICA aneurysms, but additionally our series included five pa- no surgical treatment exist – and most like- tients with rupture of primarily a undiag- ly also will never exist – that does not in- nosed (de-novo?) aneurysm. volve risk of laryngeal palsy. Surgery on most distal PICA aneurysms, and bypass- Future perspectives ing in the distal PICA will escape this risk. Etiology of VA and distal PICA aneurysms On the other hand, endovascular treat- What is specific in the VA and PICA that ment still struggles with achieving total causes them to develop a high number of occlusion of the aneurysm, or knowledge fusiform and dissecting aneurysms? In the of long-term significance of non-total oc- distal PICA, a deficiency in embryological clusion. Both methods are, many times, development is one proposal (78). In future, suboptimal in occluding dissecting VA an- it would also be interesting to examine the eurysms: for the moment the safest treat- general vasculopathy of these patients, and ment seems to be internal trapping with to compare the data to that of healthy indi- the risk of recanalization, or clip-trapping viduals as well as to patients with saccular with the risk of laryngeal palsy; both may aneurysms. Optional, of course, is to find a way to prevent formation of aneurysms. 84 Future treatment

Vkirja_viite_255246_LEHTO_.indd 82 30.3.2015 15.09 Discussion

Optimal treatment of aneurysms would be total and permanent occlusion of the aneurysm with preservation of the flow together with low risk for a neurological deficit. With most saccular aneurysms, these aims can be met. For giant and fusiform aneurysms, the solution to many challenges maybe flow-diverters. What additionally would be needed, is a revascularization method with by-far easier and faster replacement of blood flow.

Conclusion Findings of the present study are consistent with those of earlier. The VA and distal PI- CA aneurysms are rare, with an incidence of 5% of all aneurysms. The number of non- saccular aneurysms is high, comprising a third in the present series. Treatment of fusiform and dissecting aneurysms still re- quires optimization, with a high risk for laryngeal palsy in surgical treatment, and the challenge of gaining total occlusion in endovascular treatment. Despite many occa- sions of severe bleeding, most patients surviving the initial stage finally make a good recovery. ❦

85 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 83 30.3.2015 15.09 Vkirja_viite_255246_LEHTO_.indd 84 30.3.2015 15.09 Acknowledgements

This study was carried out at the Department of Neuro- surgery at Helsinki University Central Hospital between 2011 and 2015. I am grateful to all those working in Töölö Hospital for sharing their expertise and knowledge during this project and also in everyday life. I am also grateful for all the guidance and encourage- ment I have received in abundance. I am deeply thankful to Professor Juha Hernesniemi. Besides coming up with the subject of this thesis and being its supervisor, his incom- parable surgical skills gave meaning to this study. Thank you for the privilege and honor of being allowed to work in your department. I owe my gratitude to Mika Niemelä, the other supervisor of this thesis. Thank you for sharing your great expertise, for your encourage- ment, and always being available when I needed help. I am grateful to Timo Kumpulainen and Topi Siniluoto, the reviewers of this thesis, for your valuable comments that made the final result so much better. I owe so much to Riku Kivisaari. No one understands the suffering and sandwiches and Biblical images I asked you to go through when checking thousands of images for the aneurysm database and this thesis. I admire you: certainly no other person would have been strong enough to accomplish what you did.

87 Aneurysms of the vertebral and posterior inferior cerebellar arteries

Vkirja_viite_255246_LEHTO_.indd 85 30.3.2015 15.09 I am thankful to Aki Laakso for sharing I thank Tomi Metsä-Heikkilä for the beauty your vast knowledge on making science of this book. and for answering my multiple questions There would be no life without friends during this project. You were irreplaceable. and family. I thank you for your patience For Reza Dashti, I am so grateful to you in with me when I was drowning in my work. so many ways. When I came to the clinic Lotta, thank you for friendship, and also for straight from the medical school, you intro- practical help together with Rasmus Backholm duced me to neurosurgery and showed me during a crises in this project. A big thank the way to walk. You have done so much you for all my friends known in and through more for me than what I deserved. Kathos: Sanna, Tanja, Hannu and Katja, Mirka Definitely I did not create this thesis and Miikka, Laura, Topi, Toni, Sami, Anna-Leena, alone: I am more than thankful to Päivi Hanna-Kaisa, Ulla and Olli, Juha and Sofia. Koroknay-Pál, Jarno Satopää and Felix Göhre for Thank you also, Anna and Sami and your invaluable help in and friendship. family! I also want to thank the Community I am thankful to Ali Harati, Romain Billon- of Grandchamp, Sisters of Saint Andrew, Grand and Bruno Canato for all the help in the and the Taizé Community. beginning of this journey. To my family, my mother, father, Maija, Tuomo, For Behnam Rezai Jahromi, Hugo Andrade and Aino, Jaakko and Eero, thank you for your love, Ferzat Hijazy, besides all the practical help, I being there, and your continuous support. am more than grateful for sharing life and Life is beautiful with you. all the help during ups and downs in life This thesis was financially supported by and research. Surviving without you would Finnish government funding for clinical re- have been one big hell. search at Helsinki University Central Hospital I was privileged to share the experience of (EVO), Maire Taponen foundation and the making thesis with Elina Koskela and Ahmed Emil Aaltonen Foundations. ❦ Elsharkawy. Elina, thank you for long phone calls and the possibility to talk about every- thing. Ahmed, thank you for sitting hours In Helsinki, March 2015 and weeks and finally years in the same room with me, thank you for letting me try to follow your example in honesty, working, and belief in goodness. I am grateful to Carolyn Brimley Norris. Be- sides doing excellent language editing, you took time to sit for hours with me, answering all my questions, and you were always ready to help when needed. I owe you a lot. You can also be sure that I will not forget end- focus! For Eveliina Salminen, Virpi Tuukkanen, Heli Holmström, Outi Hämäläinen and Jessica Peltonen, thank you for all the practical help but especially for letting me join the life of the ”7th- floor-family“ during the long and tedious years of making the aneurysm database. 88

Vkirja_viite_255246_LEHTO_.indd 86 30.3.2015 15.09 Acknowledgements 30.3.2015 15.09 Author's contact information: Hanna Lehto Department of Neurosurgery Hospital Helsinki University Central 5 Topeliuksenkatu 00260 Helsinki Finland 2851 428 50 +358 mobile: 87560 471 9 +358 fax: e-mail: [email protected] 89 Aneurysms of the vertebral and posterior inferior cerebellar arteries Vkirja_viite_255246_LEHTO_.indd 87 Vkirja_viite_255246_LEHTO_.indd 88 30.3.2015 15.09 6. Albuquerque FC, Park M-S, Abla AA, Literature Crowley RW, Ducruet AF, McDougall CG. A reappraisal of the Pipeline embolization device for the treatment of posterior circulation aneurysms. J Neurointerv Surg. 2014. doi:10.1136/neurintsurg-2014-011340. 1. Abe T, Hagihara N, Hirohata M, Uchiyama Y, Tanaka N, Hayabuchi N. 7. Ali S, Radaideh MM, Shaibani A, Partially thrombosed vertebral artery Russell EJ, Walker MT. Persistent trigemi- aneurysm with wall enhancement treated by nal artery terminating in the posterior inferior stent-assisted coil embolization. Neurol Med cerebellar artery: case report. Neurosurgery. Chir (Tokyo). 2011;51(6):431 – 433. 2008;62(3):E746–748.

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